Groundwater Ecology And Evolution [2 ed.] 9780128191194

Citation preview

GROUNDWATER ECOLOGY AND EVOLUTION SECOND EDITION

GROUNDWATER ECOLOGY AND EVOLUTION SECOND EDITION Edited by

FLORIAN MALARD Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France

CHRISTIAN GRIEBLER University of Vienna, Department of Functional & Evolutionary Ecology, Vienna, Austria

SYLVIE RÉTAUX Paris-Saclay Institute of Neuroscience, Université Paris-Saclay and CNRS, Saclay, France

Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom Copyright © 2023 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. ISBN: 978-0-12-819119-4 For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Candice Janco Acquisitions Editor: Maria Elekidou Editorial Project Manager: Aleksandra Packowska Production Project Manager: Bharatwaj Varatharajan Cover Designer: Matthew Limbert Typeset by TNQ Technologies Front images credit: Marie Pavie, Krystel Saroul, Peter Pospisil, Robert Lepennec all rights reserved. Image on the bottom left from Zagmajster et al. (2014), Global Ecology and Biogeography 23 (10), 1135e1145.

Contents Continental scale 42 Landscape scale 44 Habitat/local scale 48 Conclusions 53 Glossary 54 Acknowledgments 55 References 55

List of contributors xi Preface xv Groundwater ecology and evolution: an introduction xvii

I

3. Physical and biogeochemical processes of hyporheic exchange in alluvial rivers

Setting the scene: groundwater as ecosystems

Daniele Tonina and John M. Buffington

Introduction 61 The hyporheic zone 64 Predicting hyporheic exchange 65 The role of hyporheic flow on water quality Conclusion 77 Acknowledgments 78 References 78

1. Hydrodynamics and geomorphology of groundwater environments Luc Aquilina, Christine Stumpp, Daniele Tonina and John M. Buffington

Introduction 3 The aquifer concept 5 Links to surface hydrology 13 Aquifer function 17 The chemical composition of groundwater 21 Chemical and nutrient fluxes in aquifers 24 Conclusion 27 Acknowledgments 28 References 28

4. Ecological and evolutionary jargon in subterranean biology  David C. Culver, Tanja Pipan and Ziga Fiser

Introduction 89 Ecological classifications 90 Colonization and speciation 95 Morphological modification for subterranean life Overall recommendations 103 Glossaries 104 Eco-Evo Glossary 104 Retired Speleobiological Glossary 105 Acknowledgments 106 References 106

2. Classifying groundwater ecosystems Anne Robertson, Anton Brancelj, Heide Stein and Hans Juergen Hahn

Introduction 39 Classification systems Global scale 42

73

41

v

99

vi

CONTENTS

II Drivers and patterns of groundwater biodiversity 5. Groundwater biodiversity and constraints to biological distribution Pierre Marmonier, Diana Maria Paola Galassi, Kathryn Korbel, Murray Close, Thibault Datry and Clemens Karwautz

Introduction 113 An overview of groundwater biodiversity 115 Physical constraints to biological distribution 122 Chemical constraints to biological distribution 125 Species interactions 128 The effect of the past: paleogeographic events and historical climates 130 Conclusion 132 Acknowledgments 133 References 133

6. Patterns and determinants of richness and composition of the groundwater fauna Maja Zagmajster, Rodrigo Lopes Ferreira, William F. Humphreys, Matthew L. Niemiller and Florian Malard

Introduction 141 Patterns of species richness 143 Patterns of species composition 152 Toward a multifaceted approach to groundwater biodiversity patterns 156 Acknowledgments 159 References 159

7. Phylogenies reveal speciation dynamics: case studies from groundwater Steven Cooper, Cene Fiser, Valerija Zaksek, Teo Delic,  Spela Borko, Arnaud Faille and William Humphreys

Introduction 165 Single colonization versus multiple colonizations from surface ancestors 168 Speciation from subterranean ancestors 169 Speciation from subterranean ancestors: likely mechanisms 171 Drivers of subterranean diversity: the role of paleoclimatic and paleogeological events 173

Synthesis and future prospects Acknowledgments 177 References 177

176

8. Dispersal and geographic range size in groundwater Florian Malard, Erik Garcia Machado, Didier Casane, Steven Cooper, Cene Fiser and David Eme

Introduction 185 Evolution of dispersal 188 Range size 193 Groundwater landscape connectivity modulates dispersal 197 Conclusion 200 Acknowledgments 201 References 201

III Roles of organisms in groundwater 9. Microbial diversity and processes in groundwater Lucas Fillinger, Christian Griebler, Jennifer Hellal, Catherine Joulian and Louise Weaver

Introduction 211 Ecological processes determining microbial community diversity and composition 213 Microbial communities and biogeochemical cycles 217 Microbial attenuation of groundwater contaminants and bottlenecks 222 Resistance and resilience of groundwater microbial communities to perturbations 227 Outlook 230 Acknowledgments 230 References 231

10. Groundwater food webs Michael Venarsky, Kevin S. Simon, Mattia Saccò, Clémentine François, Laurent Simon and Christian Griebler

Introduction 241 Basal energy dynamics in groundwater food webs 242

vii

CONTENTS

The role of habitat in groundwater food web dynamics 245 The role of food web processes in groundwater community dynamics 247 Trophic niche diversification in groundwater ecosystems 248 Future directions 249 Acknowledgments 253 References 253

11. Role of invertebrates in groundwater ecosystem processes and services Florian Mermillod-Blondin, Grant C. Hose, Kevin S. Simon, Kathryn Korbel, Maria Avramov and Ross Vander Vorste

Introduction 263 Trophic actions of invertebrates 265 Ecosystem engineering activities by invertebrates 269 Conceptual model of the role of invertebrates on ecosystem processes and consequences for ecosystem services 270 Environmental impacts on surface watere groundwater interfaces and consequences for the provision of ecosystem services by invertebrates 273 Suggestions for future research directions 275 Acknowledgments 276 References 276

IV Principles of evolution in groundwater 12. Voices from the underground: animal models for the study of trait evolution during groundwater colonization and adaptation Sylvie Rétaux and William R. Jeffery

Introduction 285 Brief historical timeline 286 Groundwater model systems 287 Troglomorphic traits 289 Timeline of troglomorphic trait evolution 293 Evolutionary developmental biology of groundwater organisms 293 Evolutionary genomics of groundwater organisms 296 Conclusions 298

Acknowledgments References 299

299

13. The olm (Proteus anguinus), a flagship groundwater species Rok Kostanjsek, Valerija Zaksek, Lilijana Bizjak-Mali and Peter Trontelj

Introduction 305 The historical rise to fame 306 Systematics and evolution 307 Molecular ecology and conservation genetics 310 Morphology and sensory systems of a groundwater top predator 313 Reproductive peculiarities 315 The overlooked part of groundwater ecology: symbioses, pathogens and parasites 317 Conservation 320 Conclusive remarks on flagship species in groundwater 322 Acknowledgments 324 References 324

14. The Asellus aquaticus species complex: an invertebrate model in subterranean evolution  Meredith Protas, Peter Trontelj, Simona Prevorcnik and Ziga Fiser

Introduction 329 Phylogeography and population structure 330 Phenotypic evolution of subterranean populations 334 Raising and breeding in the laboratory 339 Genetic basis of subterranean-related traits 340 Evolutionary development (evo-devo) 342 Comparative transcriptomics 344 Conclusions and prospect 345 Acknowledgments 346 References 346

15. Developmental and genetic basis of troglomorphic traits in the teleost fish Astyanax mexicanus Joshua B. Gross, Tyler E. Boggs, Sylvie Rétaux and Jorge Torres-Paz

The history of genetic and genomic studies of troglomorphy in Astyanax 351 Developmental basis of troglomorphy in Astyanax 357

viii

CONTENTS

Conclusions 366 Acknowledgments References 366

Acknowledgments References 432

366

16. Ecological and evolutionary perspectives on groundwater colonization by the amphipod crustacean Gammarus minus Daniel W. Fong and David B. Carlini

Introduction 373 Ecological setting and morphological variation 374 Upstream colonization of subterranean waters by Gammarus minus 377 Impetus for colonizing cave streams 378 Multiple independent colonization of cave streams 380 Evolutionary perspectives 383 Melanin pigment loss and innate immunity 387 Future directions 388 Acknowledgments 389 References 389

17. Evolutionary genomics and transcriptomics in groundwater animals Didier Casane, Nathanaelle Saclier, Maxime Policarpo, Clémentine François and Tristan Lefébure

Introduction 393 Evolution of genes and genome architecture 394 Evolution of gene expression in groundwater 405 Conclusion 410 Acknowledgments 410 References 410

432

19. Life histories in groundwater organisms Michael Venarsky, Matthew L. Niemiller, Cene Fiser, Nathanaelle Saclier and Oana Teodora Moldovan

Introduction 439 A brief overview of life history evolution, life history traits, and life table variables 442 The current conceptual model of life history evolution in groundwater species 445 Support for the current conceptual model of life history evolution in groundwater species 446 Conclusions 451 Acknowledgments 452 References 452

20. Physiological tolerance and ecotoxicological constraints of groundwater fauna Tiziana Di Lorenzo, Maria Avramov, Diana Maria Paola Galassi, Sanda Iepure, Stefano Mammola, Ana Sofia P.S. Reboleira and Frédéric Hervant

Introduction 457 Physiological tolerance of groundwater invertebrates to changing thermal conditions 458 Physiological tolerance of groundwater organisms to chemical stress 464 Physiological tolerance of groundwater organisms to light, food and oxygen variations: indications for ecotoxicological protocols 470 Conclusions 473 Acknowledgments 473 References 474

V Biological traits in groundwater 18. Dissolving morphological and behavioral traits of groundwater animals into a functional phenotype Cene Fiser, Anton Brancelj, Masato Yoshizawa,  Stefano Mammola and Ziga Fiser

Introduction 415 Habitat template 417 Morphological-behavioral functional phenotype 417 Synthesis and perspectives 430

VI Biodiversity and ecosystem management in groundwater 21. Global groundwater in the Anthropocene Daniel Kretschmer, Alexander Wachholz and Robert Reinecke

Introduction 483 Groundwater availability and distribution 484 Frameworks for sustainable use of groundwater in the Anthropocene 489

ix

CONTENTS

Anthropogenic threats to groundwater Outlook 494 Glossary 495 Acknowledgments 495 References 495

490

22. Assessing groundwater ecosystem health, status, and services Grant C. Hose, Tiziana Di Lorenzo, Lucas Fillinger, Diana Maria Paola Galassi, Christian Griebler, Hans Juergen Hahn, Kim M. Handley, Kathryn Korbel, Ana Sofia Reboleira, Tobias Siemensmeyer, Cornelia Spengler, Louise Weaver and Alexander Weigand

Introduction 501 Assessing ecosystem health and condition 503 Indicators of ecosystem health and condition 508 Defining the reference condition for groundwater ecosystems 513 Combining indicators into summary indices 515 Predicting ecosystem health and condition 516 Future directions 517 Acknowledgments 518 References 519

23. Recent concepts and approaches for conserving groundwater biodiversity Andrew J. Boulton, Maria Elina Bichuette, Kathryn Korbel, Fabio Stoch, Matthew L. Niemiller, Grant C. Hose and Simon Linke

Introduction 525 Past concepts and approaches in groundwater biodiversity conservation 527

Recent concepts and approaches in groundwater biodiversity conservation 531 Conclusion and future directions 543 Acknowledgments 545 References 545

24. Legal frameworks for the conservation and sustainable management of groundwater ecosystems Christian Griebler, Hans Juergen Hahn, Stefano Mammola, Matthew L. Niemiller, Louise Weaver, Mattia Saccò, Maria Elina Bichuette and Grant C. Hose

Introduction 551 Conservation of groundwater ecosystems and species at risk 552 Why study, assess, and protect groundwater ecosystems? 553 Legal frameworks related to groundwater ecosystems 554 Current challenges and the future of groundwater conservation 563 Acknowledgments 566 References 566

The ecological and evolutionary unity and diversity of groundwater ecosystemsdconclusions and perspective 573 Index 589

This page intentionally left blank

List of contributors Murray Close Institute of Environmental Science and Research, Christchurch, Canterbury, New Zealand

Luc Aquilina Université Rennes 1- CNRS, UMR 6118 Géosciences Rennes, Rennes, France Maria Avramov Helmholtz Zentrum München, German Research Center for Environmental Health, Institute of Groundwater Ecology, Neuherberg, Germany

Steven Cooper South Australian Museum, Adelaide, SA, Australia; The University of Adelaide, School of Biological Sciences and Australian Centre for Evolution Biology and Biodiversity, Adelaide, SA, Australia

Maria Elina Bichuette Laboratory of Subterranean Studies, Federal University of São Carlos, São Carlos, Brazil

David C. Culver Department of Environmental Science, American University, Washington, DC, United States

Lilijana Bizjak-Mali University of Ljubljana, Biotechnical Faculty, Department of Biology, Ljubljana, Slovenia

Thibault Datry INRAE, UR-RiverLY, Lyon, France Teo Delic University of Ljubljana, Biotechnical Faculty, Department of Biology, Ljubljana, Slovenia

Tyler E. Boggs Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, United States  Spela Borko University of Ljubljana, Biotechnical Faculty, Department of Biology, Ljubljana, Slovenia

Tiziana Di Lorenzo Research Institute on Terrestrial Ecosystems of the National Research Council of Italy (IRET-CNR), Florence, Italy; Emil Racovita Institute of Speleology, ClujNapoca, Romania; Centre for Ecology; Evolution and Environmental Changes (cE3c), Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal; National Biodiversity Future Center (NBFC), Palermo, Italy

Andrew J. Boulton School of Environmental and Rural Science, University of New England, Armidale, NSW, Australia Anton Brancelj Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, Gif-sur-Yvette, France; Université de Paris, UFR Sciences du Vivant, Paris, France

David Eme

INRAE, UR-RiverLY, Lyon, France

Arnaud Faille Stuttgart State Museum of Natural History, Stuttgart, Germany

John M. Buffington Rocky Mountain Research Station, US Forest Service, Boise, ID, United States

Rodrigo Lopes Ferreira Universidade Federal de Lavras (UFLA), Centro de Estudos em Biologia Subterrânea, Departamento de Ecologia e Conservação, Lavras, Minas Gerais, Brazil

David B. Carlini Department of Biology, American University, Washington, DC, United States Didier Casane Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, Gif-sur-Yvette, France; Université Paris Cité, UFR Sciences du Vivant, Paris, France

Lucas Fillinger University of Vienna, Department of Functional & Evolutionary Ecology, Vienna, Austria

xi

xii

LIST OF CONTRIBUTORS

University of Ljubljana, Biotechnical Department of Biology, Ljubljana,

William R. Jeffery Department of Biology, University of Maryland, College Park, MD, United States

University of Ljubljana, Biotechnical Department of Biology, Ljubljana,

Catherine Joulian BRGM, DEPA, Geomicrobiology and Environmental Monitoring Unit, Orléans, France

Daniel W. Fong Department of Biology, American University, Washington, DC, United States

Clemens Karwautz University of Vienna, Department of Functional & Evolutionary Ecology, Vienna, Austria

Cene Fiser Faculty, Slovenia  Ziga Fiser Faculty, Slovenia

Clémentine François Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France

Kathryn Korbel School of Natural Sciences, Macquarie University, Sydney, Australia

Diana Maria Paola Galassi Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy

Rok Kostanjsek University of Ljubljana, Biotechnical Faculty, Department of Biology, Ljubljana, Slovenia

Christian Griebler University of Vienna, Department of Functional & Evolutionary Ecology, Vienna, Austria

Daniel Kretschmer Institute of Environmental Science and Geography, University Potsdam, Potsdam, Germany

Joshua B. Gross Department of Biological Sciences, University of Cincinnati, Cincinnati, OH, United States

Tristan Lefébure Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France

Hans Juergen Hahn Institute for Environmental Sciences, University of Koblenz-Landau, Landau, Germany

Simon Linke CSIRO, Dutton Park, Brisbane, QLD, Australia

Kim M. Handley School of Biological Sciences, The University of Auckland, Auckland, New Zealand

Erik Garcia Machado Institut de Biologie Intégrative et des Systèmes (IBIS), Pavillon CharlesEugène-Marchand, Avenue de la Médecine, Université Laval Québec, Québec, Canada

Jennifer Hellal BRGM, DEPA, Geomicrobiology and Environmental Monitoring Unit, Orléans, France

Florian Malard Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France

Frédéric Hervant Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France

Stefano Mammola Molecular Ecology Group (dark-MEG), Water Research Institute (IRSA), National Research Council (CNR), VerbaniaPallanza, Italy; University of Helsinki, Finnish Museum of Natural History (LUOMUS), Helsinki, Finland

Grant C. Hose School of Natural Sciences, Macquarie University, Sydney, Australia William F. Humphreys University of Western Australia, School of Biological Sciences, Crawley, WA, Australia William Humphreys Western Australian Museum, Welshpool DC, WA, Australia Sanda Iepure Emil Racovita Institute of Speleology, Cluj-Napoca, Romania; Institutul Român de Ştiinta şi Tehnologie, Cluj-Napoca, Romania

Pierre Marmonier Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France Florian Mermillod-Blondin Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France Oana Teodora Moldovan Emil Racovitza Institute of Speleology, Cluj-Napoca, Romania

LIST OF CONTRIBUTORS

Matthew L. Niemiller Department of Biological Sciences, The University of Alabama in Huntsville, Huntsville, AL, United States Tanja Pipan ZRC SAZU, Karst Research Institute, Postojna, Slovenia Maxime Policarpo Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, Gif-sur-Yvette, France Simona Prevorcnik University of Ljubljana, Biotechnical Faculty, Department of Biology, Ljubljana, Slovenia Meredith Protas Dominican University of California, San Rafael, CA, United States Ana Sofia P.S. Reboleira Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark; Centre for Ecology, Evolution and Environmental Changes (cE3c), Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal Ana Sofia Reboleira Center for Ecology, Evolution and Environmental Changes (cE3c), Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Lisbon Portugal; Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark Robert Reinecke Institute of Environmental Science and Geography, University Potsdam, Potsdam, Germany Sylvie Rétaux Paris-Saclay Institute of Neuroscience, Université Paris-Saclay and CNRS, Saclay, France Anne Robertson School of Life & Health Sciences, University of Roehampton, London, United Kingdom Mattia Saccò Subterranean Research and Groundwater Ecology (SuRGE) Group, Trace and Environmental DNA (TrEnD) Laboratory, School of Molecular and Life Sciences, Curtin University, Perth, WA, Australia Nathanaelle Saclier ISEM, CNRS, Univ. Montpellier, IRD, EPHE, Montpellier, France; Univ Lyon, Université Claude Bernard Lyon 1,

xiii

CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France Tobias Siemensmeyer Institute for Environmental Sciences, University of Koblenz-Landau, Landau, Germany Kevin S. Simon School of Environment, University of Auckland, Auckland, New Zealand Laurent Simon Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France Cornelia Spengler Institute for Environmental Sciences, University of Koblenz-Landau, Landau, Germany Heide Stein Institute for Environmental Sciences, University of Koblenz-Landau, Landau, Germany Fabio Stoch Evolutionary Biology & Ecology, Université libre de Bruxelles, Brussels, Belgium Christine Stumpp University of Natural Resources and Life Sciences, Vienna, Department of Water, Atmosphere and Environment, Institute of Soil Physics and Rural Water Management, Vienna, Austria Daniele Tonina Center for Ecohydraulics Research, University of Idaho, Boise, ID, United States Jorge Torres-Paz Paris-Saclay Institute of Neuroscience, Université Paris-Saclay and CNRS, Saclay, France Peter Trontelj University of Ljubljana, Biotechnical Faculty, Department of Biology, Ljubljana, Slovenia Michael Venarsky Department of Biodiversity Conservation and Attractions, Kensington, WA, Australia; Australian Rivers Institute, Griffith University, Nathan, QLD, Australia Ross Vander Vorste Department of Biology, University of Wisconsin - La Crosse, La Crosse, WI, United States Alexander Wachholz Helmholtz Center for Environmental Research (UFZ), Department for Aquatic Ecosystem Analysis and Management, Magdeburg, Germany

xiv

LIST OF CONTRIBUTORS

Louise Weaver Institute of Environmental Science and Research (ESR) Christchurch, Canterbury, New Zealand

Maja Zagmajster University of Ljubljana, Biotechnical Faculty, Department of Biology, Ljubljana, Slovenia

Alexander Weigand National Museum of Natural History Luxembourg, Luxembourg

Valerija Zaksek University of Ljubljana, Biotechnical Faculty, Department of Biology, Ljubljana, Slovenia

Masato Yoshizawa University of Hawai‘i at Manoa, School of Life Sciences, Honolulu, HI, United States

Preface Since the first edition of “Groundwater Ecology” was published almost 3 decades ago, the knowledge of ecology and evolution of biodiversity in groundwater has grown tremendously. This overdue second edition does not replace the first one but is complementary to it. The first edition largely focused on case studies of groundwater ecosystems, while the second edition provides a much-needed synthesis of the current state of knowledge about the ecology and evolution of groundwater organisms. It has a stronger evolutionary emphasis, and the interplay of ecology and evolution provides the foundation for this second edition. Hence, its title is “Groundwater Ecology and Evolution.” This book covers the diversity of groundwater research conducted by ecologists and evolutionary biologists. This includes, but is not restricted to, the hydrogeological and hydrochemical attributes of groundwater habitats, the controls and patterns of groundwater biodiversity,

the role of organisms in groundwater systems, the evolutionary processes and forces driving the acquisition of subterranean biological traits, and the way these traits are differently expressed among organisms. Finally, it covers the challenges and opportunities for conservation of groundwater biodiversity and management of groundwater ecosystems. This book can be relished in its entirety or read “à la carte” because within the larger themes each chapter can stand alone. The contributors to each chapter, typically an international group of experts on a relevant topic, have successfully synthesized current research, analyzed controversies, identified knowledge gaps, and discussed future research avenues. We like to express our gratitude to all contributors and reviewers who dedicated their time and efforts to the production of this book. The editors: Florian Malard, Christian Griebler, and Sylvie Rétaux

xv

This page intentionally left blank

Groundwater ecology and evolution: an introduction Florian Malard1, Christian Griebler2 and Sylvie Rétaux3 1

Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France; 2University of Vienna, Department of Functional & Evolutionary Ecology, Vienna, Austria; 3Paris-Saclay Institute of Neuroscience, Université Paris-Saclay and CNRS, Saclay, France

Rocks, water, and life Groundwater occurs beneath the Earth’s surface in void spaces of soil, sediment, and rock formations. It is contained in geological formations known as aquifers that can hold and transmit water. Water-bearing geological strata include consolidated rocks, such as limestone and granite, as well as unconsolidated sediments, such as sand and gravel. Recent estimates of the volume of groundwater in the upper 10 km of continental crust (43.9 million km3) indicate that groundwater is the second largest reservoir of water globally, after the oceans (1.3 billion km3), and ahead of ice sheets (30.158 million km3) (Ferguson et al., 2021). However, only groundwater in the upper 1 km of the continental crust is likely to be fresh, representing an estimated volume of 15.9 million km3 (Ferguson et al., 2021). At depths greater than 1 km, groundwater is essentially brackish to saline. The estimated volume of fresh groundwater is much higher than the 0.10 million km3 of water in surface wetlands, large lakes, reservoirs, and rivers (Gleeson et al., 2016). Modern groundwaterdthe water in the first few hundred meters below ground that is less than 50 years olddrepresents a global volume of about 1.3 million km3 (0.1e5.0 million km3) (Gleeson et al., 2016). This volume dwarfs all other components of the active hydrologic cycle, namely (in order of decreasing importance) surface freshwater, soil water, atmosphere, and vegetation (Gleeson et al., 2016). Groundwater hosts a high diversity of organisms including viruses, prokaryotes (bacteria and archaea), microeukaryotes (fungi and protists), and metazoans, including invertebrates, amphibians, and fishes (Euringer and Lueders, 2008; Karwautz and Griebler, 2022; Malard, 2022; Retter and Nawaz, 2022; Schweichhart et al., 2022). Groundwater ecosystems substantially contribute to the Earth’s biodiversity and biomass. In fact, most of the global prokaryotic biomass is concentrated in the continental subsurface. Despite large uncertainties in the

xvii

xviii

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

quantification of this biomass (21e62 gigatons), it represents about 15% of the total biomass in the biosphere (Bar-on et al., 2018, but see also Magnabosco et al., 2018). The subsurface vertical extent of metazoan life is probably less than that of prokaryotes (Pedersen, 2000; Fiser et al., 2014), although nematodes were recovered in South Africa from 0.9 to 3.6 kilometer deep fractures filled with 3000e12,000-year-old palaeometeoric water (Borgonie et al., 2011). An encyclopedia of the world fauna inhabiting subterranean waters published more than 35 years ago contains more than 5500 species of metazoans (Botosaneanu, 1986). From simple extrapolations of regional species richness data, Culver and Holsinger (1992) suggested that the world subterranean metazoan fauna could represent 50,000e100,000 species, among which one third would be aquatic species. Since the world surface freshwaters accommodate approximately 125,000 animal species (Balian et al., 2008), groundwater is expected to comprise a large fraction of the Earth’s freshwater metazoan biodiversity. In Europe, the number of obligate groundwater crustaceans exceeds the number of surfacedwelling crustacean species, even though the description of groundwater species significantly lags behind that of surface species (Stoch and Galassi, 2010). The groundwater organisms and their physical environmentdwater, rocks, and sedimentsdwith which they interact constitute diverse groundwater ecosystems. Ecosystem functions, also referred to as ecosystem processes or ecological processes, correspond to the activities of organisms and the effects these activities have on their environment. In broad terms, ecosystem functions encompass the cycling of material and flow of energy. Ecosystem services are the benefits human populations obtain, directly or indirectly, from ecosystem functions (Haines-Young and Potschin, 2010). Most services provided by groundwater systems are mediated, if not entirely supported by groundwater organisms, involving microorganisms and metazoans (Boulton et al., 2008; Griebler and Avramov, 2015; Fenwick et al., 2018; Griebler et al., 2019). The capacity of aquifers to supply good-quality groundwater for various human uses without doubt depends on the activity of microorganisms and metazoans. There is compelling evidence from laboratory experiments showing that groundwater metazoans, through bioturbation and grazing of microbial biofilms, help maintain the effective porosity and hydraulic conductivity of unconsolidated sediments (Hose and Stumpp, 2019). Groundwater microorganisms exert a major control on the turnover of organic carbon and cycling of inorganic nutrients, thereby significantly contributing to the purification of groundwater along its paths from recharge to discharge areas (Griebler and Avramov, 2015). Groundwater organisms are also critical for the biodegradation of organic contaminants and elimination of pathogens, which in turn contributes to disease control (Sinton, 1984; Herman et al., 2001; Boulton et al., 2008; Griebler and Avramov, 2015). Groundwater ecosystems are open systems that strongly interact with adjacent terrestrial and surface aquatic ecosystems. Discharge of groundwater at the land surface is crucial for the continued existence of many surface terrestrial and aquatic ecosystems, commonly referred to as groundwater-dependent ecosystems (Kløve et al., 2011a,b). Conversely, the functioning and biodiversity of groundwater ecosystems depend on their linkages with terrestrial and surface aquatic ecosystems. First, in the absence of light-driven primary production, groundwater food webs depend on the supply of organic carbon from surface environments. However, there is evidence that they can also be supported to various degrees by groundwater chemolithoautotrophs (Overholt et al., 2022). Second, groundwater metazoan communities are often composed of a mix of species that show different degrees of dependence to the subterranean environment. Specialist groundwater species strictly depend on groundwater; some of them, often referred to as obligate groundwater species or

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

xix

stygobionts, complete their entire life cycle in groundwater. Generalist species (stygophiles) exploit a wide range of resources from both groundwater and surface water. Third, a difficult-to-estimate, but probably significant, proportion of obligate groundwater species is derived directly from speciation events occurring during evolutionary transitions of surface aquatic species to groundwater. Many such transitions are currently ongoing in several taxa such as crustaceans and fishes (Malard, 2022). They provide ideal models to study adaptation to a novel environment because groundwater colonizers experience drastic and sudden environmental changes (i.e. darkness and food limitation) and evolve characteristic phenotypes.

Research history in groundwater ecology and evolution There is a long history of research on the ecology and evolution of groundwater organisms. It is marked by a series of influential events, which are briefly summarized in this paragraph (Fig. 1). The first mentions of blind and depigmented cavefish (Romero, 2001) and salamander (Aljancic, 1993) date back to the 16th and 17th century, respectively. However, biospeleology, the systematic study of organisms living in caves, began at the beginning of the 20th century with the launching of the “Biospeologica” international research program (Racovitza, 1907). Until the 1960s, ecological studies were mostly restricted to caves and the main theories on the evolution of cave animals, especially those explaining the loss of structures (e.g. eyes and pigmentation), were marked by Lamarckian ideas (Vandel, 1964). Groundwater ecology started to thrive in the 1970s with the definition of groundwater ecosystems and delineation of their physical boundaries. The ecosystem concept of groundwater, originally applied to carbonate rock aquifers (see review in Rouch, 1986), was then extended to unconsolidated sedimentary aquifers (Danielopol, 1989), and now serves as a basis for the study of the flow of energy and matter in groundwater systems (Simon, 2019). Groundwater ecology gained international recognition in the 1990s when the first book dedicated to the discipline was published (Gibert et al., 1994). At roughly the same time as the emergence of groundwater ecology, in the 1960s, American speleobiologists pushed forward neoDarwinian hypotheses to explain the evolution of cave animals (Christiansen, 1961; Poulson, 1963; Barr, 1968). This endeavor culminated in the 1990s with the publication of a monograph on the importance of adaptations and natural selection in the cave amphipod Gammarus minus (Culver et al., 1995). Since 2000s, research on the ecology and evolution of subterranean organisms has entered a new era dominated by hypothesis-testing and mechanistic explanations (Fig. 1). Now, research ranges from biodiversity to biogeography, from genes to mechanisms involved in adaptation and development of specific biological traits, from the inter- and intraspecific interactions to carbon and energy flow through food webs, and from physicalechemical and structural drivers to the role of individual organisms in groundwater ecosystem functioning and services. The 2000s scientific shift had several components. First, there was an increasing number of synthesis articles (see, for example, Jeffery, 2001; Gibert and Deharveng, 2002; Danielopol et al., 2004; Wondzell, 2011; Larned, 2012; Griebler et al., 2014; Torres-Paz et al., 2018; Mammola et al., 2020; Griebler et al., 2022), special issues (Gibert and Culver, 2009; Hancock et al., 2009; Gore et al., 2018; Kowalko et al., 2020; Griebler and Hose, 2022), and books dedicated to the ecology and evolution of groundwater organisms

xx

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

FIGURE 1 A brief synopsis of research on the ecology and evolution of groundwater organisms. Numbers in parentheses refer to a nonexhaustive selection of landmark publications. (1) Racovitza (1907); (2) Vandel (1964); (3) Rouch (1986); (4) Danielopol (1989); (5) Christiansen (1961); (6) Poulson (1963); (7) Barr (1968); (8) Gibert et al. (1994); (9) Culver et al. (1995); (10) Baker et al. (2000); (11) Eme et al. (2018); (12) Hervant and Renault (2002); (13) Boulton et al. (2008); (14) Griebler and Lueders (2009); (15) Fiser et al. (2008); (16) Sbordoni et al. (2012); (17) Policarpo et al. (2021); (18) Torres-Paz et al. (2018).

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

xxi

(Chapelle, 2000; Jones and Mulholland, 2000; Wilkens et al., 2000; Griebler and Mösslacher, 2003; Romero, 2009; Culver and Pipan, 2014, 2019; Wilkens and Strecker, 2017; Moldovan et al., 2018; White et al., 2019). This period synthesized disparate results and concepts into a coherent theoretical eco-evolutionary framework for testing long-standing hypotheses and generating new ones. This theoretical framework largely benefited from the integration of concepts from several fields of research, including functional ecology (Calow, 1987), macroecology (Brown, 1995), and evolutionary developmental biology (Gilbert, 2003). Second, groundwater scientists have largely benefited from developments in biotechnology, molecular tools and data analysis for shedding new light on the functioning of groundwater food webs (Saccò et al., 2019), the relative importance of different environmental factors and evolutionary processes in shaping biodiversity patterns (Eme et al., 2018; Langille et al., 2021), and the mechanisms involved in the evolution of phenotypes (Protas et al., 2006). Third, increased connections between molecular genetics and ecology are now providing unprecedented opportunities for understanding the interplay between genes and ecological processes acting well above the organismic level. Finally, yet equally important, scientists are benefiting from the characteristic attributes of groundwater organisms and ecosystems to investigate general scientific questions that resonate well beyond the boundaries of groundwater ecology and evolution (Mammola et al., 2020). Subterranean organisms have been used as models to understand among-species variations in genome size (Lefébure et al., 2017) and rate of molecular evolution (Saclier et al., 2018), human diseases, such as degenerative eye diseases (Alunni et al., 2007), autism (Yoshizawa et al., 2018) and diabetes (Riddle et al., 2018), and the potential for life beyond Earth (Popa et al., 2012). A web of science search for the period 2019e22 indicates that approximately three percent of groundwater science articles are published in multidisciplinary journals. Contrary to the assumption that groundwater scientists contribute less than other scientists to broad-scope research questions (Griebler et al., 2014), this proportion is similar to that of other disciplines.

Groundwater research in the Anthropocene The Anthropocene refers to the time perioddbeginning potentially with the Great Acceleration in the mid-20th century (Steffen et al., 2015)dwhen the fast growing humanity started having a significant impact on the Earth’s geology and ecosystems (Crutzen, 2002). Groundwater ecosystems have not escaped human impacts. The global extraction rate of groundwater (800e1000 km3/year) exceeds that of oil by a factor of 20 (Velis et al., 2017). Groundwater is the primary source of drinking water for half of the world’s population and provides 50% of global irrigation (Famiglietti, 2014; Velis et al., 2017). The water demand for all uses continues to increase worldwide and is predicted to increase by 20%e30% by 2050 (Boretti and Rosa, 2019). In many areas of the world, groundwater extraction exceeds recharge from precipitation and surface water, thereby leading to groundwater depletion (Famiglietti, 2014). Moreover, excessive groundwater pumping has cascading effects on surface water ecosystems. De Graaf et al. (2019) estimated that environmentally critical stream flows will be reached by 2050 in approximately 42%e79% of the watersheds in which groundwater is extracted worldwide. The global groundwater crisis (Famiglietti, 2014) imposes trade-offs between various aspects

xxii

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

of human development as stated in the United Nations Sustainable Development Goals (Griggs et al., 2013) and groundwater sustainability (Velis et al., 2017). Gleeson et al. (2020) defined groundwater sustainability as “maintaining long-term, dynamically stable storage and flow of high-quality groundwater using inclusive, equitable, and long-term governance and management.” Ensuring groundwater sustainability requires maintaining groundwater ecosystem functions and associated ecosystem services over time. Groundwater depletion and pollution are ecosystem disturbances (Griebler et al., 2019) and their consequences on ecosystem functions can potentially persist well after groundwater stores have been replenished and water quality has been restored (Rouch et al., 1993). Ecosystem responses to environmental disturbances depend on the traits of organisms, their ability to move (dispersal) and adapt. Pre- and postdisturbance communities may not be functionally equivalent, potentially leading to substantial changes in ecosystem functioning and connected services. Environmental, ecological, and evolutionary research provide the basis for integrating ecosystem function and resulting services into governance and management of groundwater resources, thereby generating joint benefits to people and biodiversity (Griebler et al., 2010, 2014; Devitt et al., 2019) (Fig. 2). However, groundwater ecosystem management is yet in its infancies: a web browser search for “groundwater management” returns about one million hits vs. only one thousand hits for “groundwater ecosystem management.”

Objective of the book The objective of this book is to provide a synthesis of the current state of knowledge about the physics and biophysics of groundwater systems and the ecology and evolution of groundwater organisms. Thanks to the efforts of multiple investigators with wide-ranging expertise, this book brings together many facets of groundwater sciences ranging from hydrogeology to ecology to evolution of organisms. Bridging the gap between environmental, ecological, and evolutionary studies can foster the development of groundwater management practices that is needed to preserve the sustainability of groundwater ecosystems and their services to society.

Audience Groundwater Ecology and Evolution, second edition, is primarily intended for an audience of graduate students, postgraduate students, and academic researchers involved in the study of groundwater biodiversity, the function of groundwater ecosystems, and the evolution of groundwater organisms. This book not only represents an excellent resource for teaching groundwater ecology at the university level, but also provides fascinating case studies of evolution in caves for teaching evolutionary biology. Despite its focus on groundwater, this book is also highly relevant for general biologists. Groundwater ecosystems are excellent model systems to study general principles: in evolution, the mechanisms resulting in adaptation to a novel environment, in physiology, the mechanisms supporting life in extreme environments, and, in ecology, the importance of biodiversity for nutrient cycling at sedimentary interfaces. Groundwater is a crucial resource to humans. This book provides water managers

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

xxiii

FIGURE 2 Groundwater research in the Anthropocene.

with key information on ecosystem management practices that contribute to maintaining groundwater sustainability in the face of future resource-use scenarios. We hope that the diverse readers will make frequent use of this book in basic science, applied science, and teaching.

Structure and content of the book This book is composed of 24 chapters grouped into six sections. The first section (Chapters 1e4) sets the environmental stage by describing the physical attributes of groundwater ecosystems. It also provides a glossary as part of Chapter 4 that revisits the specialized terminology used in subterranean biology. Chapter 1 describes the physical and hydrodynamic properties of aquifers, their linkages with surface water, groundwater age, the flow of groundwater, and transport of solutes and particulate matter. In addition, it provides insights into the chemical composition of groundwater, watererock interactions, and chemical fluxes

xxiv

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

in aquifers. Chapter 2 focuses on the flow of water in the hyporheic zone of alluvial rivers, a functionally important transitional habitat between surface and ground waters. It describes operative definitions of the hyporheic zone, models for predicting hyporheic flow paths across different spatial scales, and the influence of hyporheic flow on water quality. Chapter 3 reviews existing classification systems for groundwater ecosystems at four hierarchical spatial scalesdglobal, continental, landscape, and localdand emphasizes the importance of classification schemes for integrating groundwater ecosystems into the monitoring of freshwater aquatic ecosystems. Chapter 4 proposes to replace the specialized terminology used in subterranean biology with a more general ecological and evolutionary terminology. The specialized terminologies that are examined are those of ecological classifications of groundwater organisms, transitions of surface aquatic species to groundwater, and biological traits of obligate groundwater species. The next four chapters in Section 2 review the controls and patterns of groundwater biodiversity. Chapter 5 provides an account of the taxonomic diversity of living forms in groundwater including viruses, prokaryotes, microeukaryotes, and metazoans. It documents the main constraints for biological distributions in groundwater, including physical and chemical constraints, biotic interactions, and the effects of past constraints linked to major paleogeographic events and historical climates. Chapter 6 gives an overview of the most striking features of patterns in species richness and taxonomic composition of the obligate groundwater fauna at regional to continental scales. It emphasizes patterns that are common enough among taxonomic groups and continents to be potentially recognized as “rules” and reports on the most probable combination of mechanisms shaping these patterns. The next two chapters focus on speciation and dispersal, two of the three processes that ultimately determine the number of species in a region. The third process, extinction, unfortunately is difficult to quantify in the absence of fossil records among groundwater species. Chapter 7 provides phylogenetic and phylogeographic studies of representative groundwater species-rich taxa and discusses the processes that have led to their speciation. It focuses on the evidence for speciation from surface aquatic ancestors versus subterranean speciation, where species evolve from groundwater ancestors within groundwater environments. Chapter 8 introduces dispersal in groundwater and highlights the factors controlling the eco-evolutionary dynamics of dispersal that are relevant for understanding species-range dynamics. It reports on the main barriers to dispersal of groundwater organisms and provides a case study showing how groundwater-landscape resistance controls the movement of organisms. Section 3 contains three chapters that describe the roles of organisms in groundwater ecosystems. Chapter 9 provides an overview of the factors that determine the diversity and composition of microbial communities in groundwater, the resistance and resilience of microbial communities to disturbances, and their role in key biogeochemical processes including the cycling of organic matter and nutrients, and natural attenuation of contaminants. Chapter 10 begins with a discussion of basal energy dynamics in groundwater foodwebs that covers both organic matter dynamics as well as chemolithoautotrophic primary production. Then, it explores the role habitats play in structuring the inputs and processing of matter and energy and the influence of various food-web mechanisms on trophic-niche diversification and relative importance of bottom-up and top-down processes. Chapter 11 shows how invertebrates influence groundwater ecosystem function through their trophic interactions with biofilms and nontrophic actions that engineer the physical environment.

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

xxv

These trophic and engineering activities are modulated by habitat factors, in particular by the strength of surface wateregroundwater exchanges, and they are sensitive to human-driven environmental disturbances. Section 4 is devoted to developmental and evolutionary processes related to the acquisition of subterranean biological traits. The section starts with an introduction (Chapter 12) that gives an overview at the organismal level of recent research documenting the variety of troglomorphic traits specific to groundwater animals. It also introduces the fields and principles of evolutionary developmental biology (EvoDevo) and comparative genomics for the study of trait evolution in the dark. Chapters 13e16 give detailed presentations of emblematic model systems that have been the most studied so far and have brought most insights into the evolution of troglomorphy: the amphibian “olm” Proteus anguinus (Chapter 13), the isopod crustacean Asellus aquaticus (Chapter 14), the teleost fish Astyanax mexicanus (Chapter 15), and the amphipod crustacean G. minus (Chapter 16). The section ends with Chapter 17, which summarizes our current understanding of the evolution of gene sequences, gene expression, and genome architecture associated with surface to groundwater transition. Section 5 summarizes the organismal-level research presented in the previous section by providing an overview of variation in morphological, behavioral, life-history, and physiological traits among groundwater organisms. Chapter 18 considers six general aspects of the morphological and behavioral phenotype, namely sensory input, locomotion, feeding, (micro)habitat choice, reproduction, and antipredator response. It introduces the “many-to-one relationship of form and function” principle, stating that enhancement of functional performance is possible either through morphological or behavioral changes, and proposes that this principle can explain variation in phenotypes among habitats, accounting for different trade-offs. Chapter 19 explores the current state of life-history research in groundwater fauna, including a brief review of life-history evolution, life-history traits, and life-table variables. The chapter outlines the current conceptual model of life-history evolution in groundwater species and reviews the support for this model, acknowledging that most inferences are from a few model taxa. Chapter 20 is devoted to the study of physiological tolerance of groundwater species. This includes the responses of organisms to light, food, and oxygen variations and their ability to cope with temperature changes and chemical contamination. Data are examined within the contexts of ecological risk-assessment of groundwater, global warming, and decreasing groundwater quality. Section 6, the last section of the book, shows how knowledge derived from multiple research foci (Sections 1e5) can be used to manage groundwater biodiversity and ecosystem services in the face of future groundwater resource-use scenarios. Chapter 21 provides a global perspective of the crucial importance of groundwater resources, for both humans and ecosystems, and threats to these resources due to unsustainable use in the Anthropocene. Chapter 22 introduces current schemes for the assessment of groundwater ecosystem health, status, and services. These include conventional groundwater-assessment methods in the fields of community ecology, functional ecology, and ecotoxicology. It concludes with a discussion on future directions and knowledge gaps. Chapter 23 deals with recent concepts and approaches for conserving groundwater biodiversity, while Chapter 24 summarizes existing legal frameworks for the protection and conservation of groundwater organisms and ecosystems.

xxvi

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

We finish the book with a conclusion chapter that identifies knowledge gaps, priorities in basic research, and challenges for the governance and management of groundwater ecosystems.

Acknowledgments We like to express our gratitude to all contributors and reviewers who dedicated their time and effort to the production of this book. This books represents the work of 78 contributors from 56 research laboratories in 17 countries. We like to thank Aleksandra Packowska, Editorial Project Manager, and Bharatwaj Varatharajan, Production Manager, for their continuous support throughout the realization of the book. We thank Björn Wissel for proofreading and English-language editing the General Introduction.

References Aljancic, M., Bulog, B., Kranjc, A., Habic, P., Josipovic, D., Sket, B., Skoberne, P., 1993. Proteus: The Mysterious Ruler of Karst Darkness. Speleo Projects. Caving Publications International, Ljubiana, Slovenia. Alunni, A., Menuet, A., Candal, E., Pénigault, J.B., Jeffery, W.R., Rétaux, S., 2007. Developmental mechanisms for retinal degeneration in the blind cavefish Astyanax mexicanus. Journal of Comparative Neurology 505 (2), 221e233. Baker, M.A., Dahm, C.N., Valett, H.M., 2000. Anoxia, anaerobic metabolism, and biogeochemistry of the streamwater-ground-water interface. In: Jones, J.B., Mulholland, P.J. (Eds.), Streams and Groundwaters. Academic Press, San Diego, California, pp. 259e283. Balian, E.V., Segers, H., Lévèque, C., Martens, K., 2008. The freshwater animal diversity assessment: an overview of the results. Hydrobiologia 595, 627e637. Bar-On, Y.M., Phillips, R., Milo, R., 2018. The biomass distribution on Earth. Proceedings of the National Academy of Sciences of the United States of America 115 (25), 6506e6511. Barr, T.C., 1968. Cave ecology and the evolution of troglobites. Evolutionary Biology 2, 35e102. Boretti, A., Rosa, L., 2019. Reassessing the projections of the world water development report. NPJ Clean Water 2, 15. Borgonie, G., Garcia-Moyano, A., Litthauer, D., Bert, W., Bester, A., van Heerden, E., Möller, C., Erasmus, M., Onstott, T.C., 2011. Nematoda from the terrestrial deep subsurface of South Africa. Nature 474, 79e82. Botosaneanu, L., 1986. Stygofauna Mundi: A Faunistic, Distributional, and Ecological Synthesis of the World Fauna Inhabiting Subterranean Waters. E.J. and Dr. W. Backhuys, Leiden, The Netherlands. Boulton, A.J., Fenwick, G.D., Hancock, P.J., Harvey, M.S., 2008. Biodiversity, functional roles and ecosystem services of groundwater invertebrates. Invertebrate Systematics 22, 103e116. Brown, J.H., 1995. Macroecology. The University of Chicago Press, Chicago. Calow, P., 1987. Towards a definition of functional ecology. Functional Ecology 1, 57e61. Chapelle, F.H., 2000. Ground-Water Microbiology and Geochemistry, second ed. Wiley. Christiansen, K.A., 1961. Convergence and parallelism in cave entomobryinae. Evolution 15, 288e301. Crutzen, P.J., 2002. Geology of mankind. Nature 415, 23. Culver, D.C., Pipan, T., 2014. Shallow Subterranean Habitats. Ecology, Evolution, and Conservation. Oxford University Press, Oxford. Culver, D.C., Pipan, T., 2019. The Biology of Caves and Other Subterranean Habitats, second ed. Oxford University Press, Oxford. Culver, D.C., Kane, T.C., Fong, D.W., 1995. Adaptation and Natural Selection in Caves: The evolution of Gammarus minus. Harvard University Press, Cambridge. Danielopol, D.L., 1989. Groundwater fauna associated with riverine aquifers. Journal of the North American Benthological Society 8 (1), 18e35. Danielopol, D.L., Gibert, J., Griebler, C., Gunatilaka, A., Hahn, H.J., Messana, G., Notenboom, J., Sket, B., 2004. Incorporating ecological perspectives in European groundwater management policy. Environmental Conservation 31 (3), 185e189. de Graaf, I.E.M., Gleeson, T., van Beek, L.P.H., Sutanudjaja, E.H., Bierkens, M.F.P., 2019. Environmental flow limits to global groundwater pumping. Nature 573, 90e94.

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

xxvii

Devitt, T.J., Wright, A.M., Cannatella, D.C., Hillis, D.M., 2019. Species delimitation in endangered groundwater salamanders: Implications for aquifer management and biodiversity conservation. Proceedings of the National Academy of Sciences of the United States of America 116 (7), 2624e2633. Eme, D., Zagmajster, M., Delic, T., Fiser, C., Flot, J.-F., Konecny-Dupré, L., Pálsson, S., Stoch, F., Zaksek, V., Douady, C.J., Malard, F., 2018. Do cryptic species matter in macroecology? Sequencing European groundwater crustaceans yields smaller ranges but does not challenge biodiversity determinants. Ecography 41, 424e436. Euringer, K., Lueders, T., 2008. An optimised PCR/T-RFLP fingerprinting approach for the investigation of protistan communities in groundwater environments. Journal of Microbiological Methods 75 (2), 262e268. Famiglietti, J.S., 2014. The global groundwater crisis. Nature Climate Change 4, 945e948. Fenwick, G., Greenwood, M., Williams, E., Milne, J., Watene-Rawiri, E., 2018. Groundwater Ecosystems: Functions, Values, Impacts and Management. NIWA Report 2018184CH, Horizons Regional Council, Palmerston North, New Zealand. Ferguson, G., McIntosh, J.C., Warr, O., Sherwood Lollar, B., Ballentine, C.J., Famiglietti, J.S., Kim, J.-H., Michalski, J.R., Mustard, J.F., Tarnas, J., McDonnell, J.J., 2021. Crustal groundwater volumes greater than previously thought. Geophysical Research Letters 48 e2021GL093549. Fiser, C., Sket, B., Trontelj, P., 2008. A phylogenetic perspective on 160 years of troubled taxonomy of Niphargus (Crustacea: Amphipoda). Zoologica Scripta 37 (6), 665e680. Fiser, C., Pipan, T., Culver, D.C., 2014. The vertical extent of groundwater metazoans: an ecological and evolutionary perspective. BioScience 64 (11), 971e979. Gibert, J., Culver, D.C., 2009. Assessing and conserving groundwater biodiversity: an introduction. Freshwater Biology 54, 639e648. Gibert, J., Deharveng, L., 2002. Subterranean ecosystems: a truncated functional biodiversity. BioScience 52 (6), 473e481. Gibert, J., Danielopol, D.L., Stanford, J.A., 1994. Groundwater Ecology. Academic Press, San Diego, USA. Gilbert, S.F., 2003. The morphogenesis of evolutionary developmental biology. International Journal of Developmental Biology 47 (7-8), 467e477. Gleeson, T., Befus, K.M., Jasechko, S., Luijendijk, E., Cardenas, M.B., 2016. The global volume and distribution of modern groundwater. Nature Geoscience 9 (2), 161e167. Gleeson, T., Cuthbert, M., Ferguson, G., Perrone, D., 2020. Global groundwater sustainability, resources, and systems in the Anthropocene. Annual Review of Earth and Planetary Sciences 48, 431e463. Gore, A.V., Rohner, N., Rétaux, S., Jeffery, W.R., 2018. Seeing a bright future for a blind fish. Developmental Biology 441 (2), 207e208. Griebler, C., Avramov, M., 2015. Groundwater ecosystem services: a review. Freshwater Science 34 (1), 355e367. Griebler, C., Hose, G.C., 2022. Section introduction: groundwater sciences in limnology. In: Mehner, T., Tockner, K. (Eds.), Encyclopedia of Inland Waters, second ed. Elsevier, pp. 303e305. Griebler, C., Lueders, T., 2009. Microbial biodiversity in groundwater ecosystems. Freshwater Biology 54 (4), 649e677. Griebler, C., Stein, H., Kellermann, C., Berkhoff, S., Brielmann, H., Schmidt, S., Selesi, D., Steube, C., Fuchs, A., Hahn, H.J., 2010. Ecological assessment of groundwater ecosystemsevision or illusion? Ecological Engineering 36 (9), 1174e1190. Griebler, C., Malard, F., Lefébure, T., 2014. Current developments in groundwater ecology - from biodiversity to ecosystem function and services. Current Opinion in Biotechnology 27, 159e167. Griebler, C., Avramov, M., Hose, G., 2019. Groundwater ecosystems and their services: current status and potential risks. In: Schröter, M., Bonn, A., Klotz, S., Seppelt, R., Baessler, C. (Eds.), Atlas of Ecosystem Services. Springer, Cham, pp. 197e203. Griebler, C., Fillinger, L., Karwautz, C., Hose, G.C., 2022. Knowledge gaps, obstacles, and research frontiers in groundwater microbial ecology. In: Mehner, T., Tockner, K. (Eds.), Encyclopedia of Inland Waters, second ed. Elsevier, pp. 611e624. Griebler, C., Mösslacher, F., 2003. Grundwasser-Ökologie (Groundwater Ecology). UTB-Fakultas Verlag, Wien. Griggs, D., Stafford-Smith, M., Gaffney, O., Rockström, J., Öhman, M.C., Shyamsundar, P., Steffen, W., Glaser, G., Kanie, N., Noble, I., 2013. Sustainable development goals for people and planet. Nature 495 (7441), 305e307. Haines-Young, R., Potschin, M., 2010. The links between biodiversity, ecosystem services and human well-being. In: Raffaelli, D.G., Frid, C.L.J. (Eds.), Ecosystem Ecology: A New Synthesis. Cambridge University Press, British Ecological Society, pp. 110e139.

xxviii

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

Hancock, P.J., Hunt, R.J., Boulton, A.J., 2009. Preface: hydrogeoecology, the interdisciplinary study of groundwater dependent ecosystems. Hydrogeology Journal 17, 1e3. Hervant, F., Renault, D., 2002. Long-term fasting and realimentation in hypogean and epigean isopods: a proposed adaptive strategy for groundwater organisms. The Journal of Experimental Biology 205 (14), 2079e2087. Culver, D.C., Holsinger, J.R., 1992. How many species of troglobites are there? NSS Bulletin 54, 79e80. Herman, J.S., Culver, D.C., Salzman, J., 2001. Groundwater ecosystems and the service of water purification. Stanford Environmental Law Journal 20, 479e495. Hose, G.C., Stumpp, C., 2019. Architects of the underworld: bioturbation by groundwater invertebrates influences aquifer hydraulic properties. Aquatic Sciences 81, 20. Jeffery, W.R., 2001. Cavefish as a model system in evolutionary developmental biology. Developmental Biology 231, 1e12. Jones, J.B., Mulholland, P.J., 2000. Streams and Ground Waters. Academic Press, San Diego, California. Karwautz, C., Griebler, C., 2022. Microbial biodiversity in groundwater ecosystems. In: Mehner, T., Tockner, K. (Eds.), Encyclopedia of Inland Waters, Second ed. Elsevier, pp. 397e411. Kløve, B., Ala-aho, P., Bertrand, G., Boukalova, Z., Ertürk, A., Goldscheider, N., Ilmonen, J., Karakaya, N., Kupfersberger, H., Kvœrner, J., Lundberg, A., Mileusnic, M., Moszczynska, A., Muotka, T., Preda, E., Rossi, P.,  Siergieiev, D., Simek, J., Wachniew, P., Angheluta, V., Widerlund, A., 2011a. Groundwater dependent ecosystems. Part I: hydroecological status and trends. Environmental Science and Policy 14 (7), 770e781. Kløve, B., Allan, A., Bertrand, G., Druzynska, E., Ertürk, A., Goldscheider, N., Henry, S., Karakaya, N., Karjalainen, T.P., Koundouri, P., Kupfersberger, H., Kvœrner, J., Lundberg, A., Muotka, T., Preda, E., PulidoVelazquez, M., Schipper, P., 2011b. Groundwater dependent ecosystems. Part II. Ecosystem services and management in Europe under risk of climate change and land use intensification. Environmental Science and Policy 14 (7), 782e793. Kowalko, J.E., Franz-Odendaal, T.A., Rohner, N., 2020. Introduction to the special issuedcavefishdadaptation to the dark. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 334, 393e396. Langille, B.L., Hyde, J., Saint, K.M., Bradford, T.M., Stringer, D.N., Tierney, S.M., Humphreys, W.F., Austin, A.D., Cooper, S.J.B., 2021. Evidence for speciation underground in diving beetles (Dytiscidae) from a subterranean archipelago. Evolution 75 (1), 166e175. Larned, Z.T., 2012. Phreatic groundwater ecosystems: research frontiers for freshwater ecology. Freshwater Biology 57, 885e906. Lefébure, T., Morvan, C., Malard, F., François, C., Konecny-Dupré, L., Guéguen, L., Weiss-Gayet, M., SeguinOrlando, A., Ermini, L., Der Sarkissian, C., Charrier, N.P., Eme, D., Mermillod-Blondin, F., Duret, L., Vieira, C., Orlando, L., Douady, C.J., 2017. Less effective selection leads to larger genomes. Genome Research 27, 1016e1028. Magnabosco, C., Lin, L.-H., Dong, H., Bomberg, M., Ghiorse, W., Stan-Lotter, H., Pedersen, K., Kieft, T.L., van Heerden, E., Onstott, T.C., 2018. The biomass and biodiversity of the continental subsurface. Nature Geoscience 11, 707e717. Malard, F., 2022. Groundwater Metazoans. In: Mehner, T., Tockner, K. (Eds.), Encyclopedia of Inland Waters, second ed. Elsevier, pp. 474e487. Mammola, S., Amorim, I.R., Bichuette, M.E., Borges, P.A.V., Cheeptham, N., Cooper, S.J.B., Culver, D.C.,  Fong, D.W., Griebler, C., Jeffery, W.R., Jugovic, J., Deharveng, L., Eme, D., Ferreira, R.L., Fiser, C., Fiser, Z., Kowalko, J.E., Lilley, T.M., Malard, F., Manenti, R., Martínez, A., Meierhofer, M.B., Niemiller, M.L., Northup, D.E., Pellegrini, T.G., Pipan, T., Protas, M., Reboleira, A.S.P.S., Venarsky, M.P., Wynne, J.J., Zagmajster, M., Cardoso, P., 2020. Fundamental research questions in subterranean biology. Biological Reviews 95, 1855e1872. Moldovan, O.T., Kovác, L., Halse, S., 2018. Cave Ecology. Springer Nature, Cham, Switzerland. Overholt, W.A., Trumbore, S., Xu, X., Bornemann, T.L.V., Probst, A.J., Krüger, M., Herrmann, M., Thamdrup, B., Bristow, L.A., Taubert, M., Schwab, V.F., Hölzer, M., Marz, M., Küsel, K., 2022. Carbon fixation rates in groundwater similar to those in oligotrophic marine systems. Nature Geoscience 15, 561e567. Pedersen, K., 2000. Exploration of deep intraterrestrial microbial life: current perspectives. FEMS Microbiology Letters 185, 9e16. Policarpo, M., Fumey, J., Lafargeas, P., Naquin, D., Thermes, C., Naville, M., Dechaud, C., Volff, J.-N., Cabau, C., Klopp, C., Møller, P.R., Bernatchez, L., García-Machado, E., Rétaux, S., Casane, D., 2021. Contrasting gene decay in subterranean vertebrates: insights from cavefishes and fossorial mammals. Molecular Biology and Evolution 38 (2), 589e605.

GROUNDWATER ECOLOGY AND EVOLUTION: AN INTRODUCTION

xxix

Popa, R., Smith, A.R., Popa, R., Boone, J., Fisk, M., 2012. Olivine-respiring bacteria isolated from the rock-ice interface in a lava-tube cave, a Mars analog environment. Astrobiology 12 (1), 9e18. Poulson, T.L., 1963. Cave adaptation in amblyopsid fishes. The American Midland Naturalist 70, 257e290. Protas, M.E., Hersey, C., Kochanek, D., Zhou, Y., Wilkens, H., Jeffery, W.R., Zon, L.I., Borowsky, R., Tabin, C.J., 2006. Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nature Genetics 38 (1), 107e111. Racovitza, E.G., 1907. Essai sur les problèmes biospéologiques. Archives de Zoologie Expérimentale et Générale 6, 371e488. Retter, A., Nawaz, A., 2022. The groundwater mycobiome: fungal diversity in terrestrial aquifers. In: Mehner, T., Tockner, K. (Eds.), Encyclopedia of Inland Waters, Second ed. Elsevier, pp. 385e396. Riddle, M.R., Aspiras, A.C., Gaudenz, K., Peuß, R., Sung, J.Y., Martineau, B., Peavey, M., Box, A.C., Tabin, J.A., McGaugh, S., Borowsky, R., Tabin, C.J., Rohner, N., 2018. Insulin resistance in cavefish as an adaptation to a nutrient-limited environment. Nature 555, 647e651. Romero, A., 2001. Scientists prefer them blind: the history of hypogean fish research. Environmental Biology of Fishes 62, 43e71. Romero, A., 2009. Cave Biology. Life in Darkness. Cambridge University Press, Cambridge. Rouch, R., 1986. Sur l’écologie des eaux souterraines dans le karst. Stygologia 2 (4), 352e398. Rouch, R., Pitzalis, A., Descouens, A., 1993. Effets d’un pompage à gros débit sur le peuplement des Crustacés d’un aquifère karstique. Annales de Limnologie 29, 15e29. Saccò, M., Blyth, A., Bateman, P.W., Hua, Q., Mazumder, D., White, N., Humphreys, W.F., Laini, A., Griebler, C., Grice, K., 2019. New light in the darkda proposed multidisciplinary framework for studying functional ecology of groundwater fauna. Science of the Total Environment 662, 963e977. Saclier, N., François, C.M., Konecny-Dupré, L., Lartillot, N., Guéguen, L., Duret, L., Malard, F., Douady, C.J., Lefébure, T., 2018. Life history traits impact the nuclear rate of substitution but not the mitochondrial rate in isopods. Molecular Biology and Evolution 35, 2900e2912. Sbordoni, V., Allegrucci, G., Cesaroni, D., 2012. Population structure. In: White, W.B., Culver, D.C. (Eds.), Encyclopedia of Caves, Second edition. Academic/Elsevier Press, Amsterdam, the Netherlands, pp. 608e618. Schweichhart, J.S., Pleyer, D., Winter, C., Retter, A., Griebler, C., 2022. Presence and role of prokaryotic viruses in groundwater environments. In: Mehner, T., Tockner, K. (Eds.), Encyclopedia of Inland Waters, Second ed. Elsevier, pp. 373e384. Simon, K.S., 2019. Cave ecosystems. In: White, W.B., Culver, D.C., Pipan, T. (Eds.), Encyclopedia of Caves. Academic Press, London, UK, pp. 223e226. Sinton, L.W., 1984. The macroinvertebrates in a sewage-polluted aquifer. Hydrobiologia 119, 161e169. Steffen, W., Broadgate, W., Deutsch, L., Gaffney, O., Ludwig, C., 2015. The trajectory of the Anthropocene: the great acceleration. The Anthropocene Review 2 (1), 81e98. Stoch, F., Galassi, D.M.P., 2010. Stygobiotic crustacean species richness: a question of numbers, a matter of scale. Hydrobiologia 653, 217e234. Torres-Paz, J., Hyacinthe, C., Pierre, C., Rétaux, S., 2018. Towards an integrated approach to understand Mexican cavefish evolution. Biology Letters 14 (8), 20180101. Vandel, A., 1964. Biospéologie: la biologie des animaux cavernicoles. Gauthier-Villars, Paris. Velis, M., Conti, K.I., Biermann, F., 2017. Groundwater and human development: synergies and trade-offs within the context of the sustainable development goals. Sustainability Science 12, 1007e1017. White, W.B., Culver, D.C., Pipan, T., 2019. Encyclopedia of Caves. Academic Press, London, UK. Wilkens, H., Strecker, U., 2017. Evolution in the Dark. Darwin’s Loss Without Selection. Springer, Cham. Wilkens, H., Culver, D.C., Humphreys, W.F., 2000. Subterranean ecosystems. Ecosystems of the world, vol 30. Elsevier, Amsterdam. Wondzell, S.M., 2011. The role of the hyporheic zone across stream networks. Hydrological Processes 25 (22), 3525e3532. Yoshizawa, M., Settle, A., Hermosura, M.C., Tuttle, L.J., Cetraro, N., Passow, C.N., McGaugh, S.E., 2018. The evolution of a series of behavioral traits is associated with autism-risk genes in cavefish. BMC Evolutionary Biology 18, 89.

This page intentionally left blank

S E C T I O N I

Setting the scene: groundwater as ecosystems

This page intentionally left blank

C H A P T E R

1 Hydrodynamics and geomorphology of groundwater environments Luc Aquilina1, Christine Stumpp2, Daniele Tonina3 and John M. Buffington4 1

Université Rennes 1- CNRS, UMR 6118 Géosciences Rennes, Rennes, France; 2University of Natural Resources and Life Sciences, Vienna, Department of Water, Atmosphere and Environment, Institute of Soil Physics and Rural Water Management, Vienna, Austria; 3Center for Ecohydraulics Research, University of Idaho, Boise, ID, United States; 4Rocky Mountain Research Station, US Forest Service, Boise, ID, United States

Introduction Within the global water cycle, the groundwater pool represents a substantial volume of water, containing approximately 8,000-23,000•103 km3 (Abbott et al., 2019). Annual groundwater discharge to the ocean (0.1e6.5•103 km3/year) is two to three orders of magnitude smaller than oceanic evaporation (350e510•103 km3/year), which initiates the continental part of the water cycle through atmospheric condensation and landward precipitation (88e120•103 km3/year). The other segments of the water cycle are part of our daily life: the clouds in the sky, the polar ice seen from satellites and the snow, closer to us, the rivers we like to walk along, and the lakes where we go fishing and swimming. Conversely, the underground part of the water cycle remains poorly known to the general public. It is the invisible part of the water cycle. In fact, for many people, the notion of groundwater is generally associated with the idea of an underground lake or river. Instead, groundwater is a spongelike hydrologic system that occupies an extensive network of voids in near-surface (crustal) rocks of the continents and ocean floor. While groundwater systems are understood conceptually, less is often known about the specific movement of water through the subsurface system and the associated annual water cycle. Groundwater has long been difficult to comprehend in its entirety due to its subterranean nature and difficulty of access. Geologic maps offer clues for determining where groundwater may occur as a function of different rock types, sedimentary deposits, and surface topography,

Groundwater Ecology and Evolution, Second Edition https://doi.org/10.1016/B978-0-12-819119-4.00014-7

3

© 2023 Elsevier Inc. All rights reserved.

4

1. Hydrodynamics and geomorphology of groundwater environments

but the spatiotemporal extent of groundwater can only be measured from boreholes/wells and cave/spring systems, which are typically limited to a relatively small number of locations. The underground hydrologic system is dynamic, made up of numerous flow paths (Fig. 1.1). The nature of these flows is complex, in response to the strong heterogeneity (spatial variability) of geological formations and, in turn, their ability to hold and transfer water (permeability). The soil (top layer of the sediment) constitutes the first compartment that controls flows feeding the groundwater system as a result of precipitation and snowmelt that percolate into the soil. Within a given groundwater system, we can find very fast flows, as well as areas with extremely slow flows. These variations can exist both on a regional scale and on a microscopic scale, with variations in flow controlling the physical and chemical interactions between water and rock. The physical control of water fluxes and the chemical control of elements are therefore intrinsically coupled. Observed linkages between surface water and groundwater provide further information about the extent and function of the groundwater system, with recent studies emphasizing the need to evaluate river systems within the context of groundwater processes. For example, springs, which are a direct emergence of groundwater onto the landscape, can have important controls on headwater portions of the surface water system and downstream water quality (Peterson et al., 2001; Alexander et al., 2007; Meyer et al., 2007; Soulsby et al., 2007; Rhoades et al., 2021). Throughout their course, rivers also receive diffuse flows from the underground environment that modulate physical conditions. In turn, rivers drive complex exchanges of water between the surface and subsurface hydrologic systems. Consequently, surface water and groundwater are extremely dynamic, integrated systems. Groundwater resources have become a subject of concern in the Anthropocene (the current geologic epoch in which humans have substantially altered physical and ecological processes (Crutzen, 2002), especially regarding climate change and pollution. Climate-driven increases in temperature and evapotranspiration may limit future groundwater volumes and the extent of groundwater flow. Weakening groundwater flows can have severe impacts on surface systems and may increase the length and occurrence of droughts. Drought, which occurs in nearly all regions, has affected more people worldwide in the last 40 years than any other natural hazard. The effects of water scarcity can manifest through environmental crises, as droughts may induce tipping points (Otto et al., 2020). As such, active research currently focuses on the effects of climate change on groundwater systems (Amanambu et al., 2020) given that a large number of human populations may have difficulty accessing drinking water under future climate scenarios. Human activities also can have major effects on the water quality of groundwater systems. Intensive agriculture can cause diffuse pollution of nitrate, creating extensive eutrophication (Vitousek et al., 1997; Tilman et al., 2001). Other pollutants entering groundwater systems, such as endocrine disruptors, nanoparticles, and microplastics, have become a major concern due to their impact on both human life and biodiversity (Kremen et al., 2002; Gallo et al., 2018). Groundwater ecosystems also host a large variety of organisms that dwell in open spaces within the underground material, ranging from small pores or cracks to large voids and tunnels that are typically present in karst landscapes (e.g., limestone caverns) and lava tubes. The flows that traverse the underground environment also control the supply of nutrients accessible to living organisms. Porosity and flow, therefore, condition the subsurface living world and constitute an extremely diverse set of habitats in which physical, chemical, and biological systems are intimately interconnected. I. Setting the scene: groundwater as ecosystems

The aquifer concept

5

The aim of this chapter is to describe the physical and chemical principles that characterize these underground environments. Specifically, we review the physical basis of aquifers (groundwater reservoirs), their hydrodynamics, and hydrogeological parameters (porosity and permeability) that collectively define different types of aquifers. We explore the relationships between groundwater and surface water and define how aquifers function in terms of (1) groundwater flow and the transport of solutes and particulate matter; (2) groundwater age, which affects ecosystem processes, physical and biological relations, and groundwater resources; and (3) modeling of the above processes. We also consider the chemical composition of groundwater and the origin of compounds and watererock interactions that influence water quality. Finally, we discuss chemical and nutrient fluxes in aquifers and biogeochemical reactions, with a focus on oxygen and nitrogen.

The aquifer concept Most rocks, soils, and sediments near the surface of the earth have a certain degree of porosity caused by voids and fractures and, thus, are referred to as porous media. The ability of porous media to transmit water (permeability) depends on having connected pores. Permeable subsurface lithologies that contain extensive bodies of groundwater are termed aquifers. The upper surface of the aquifer is known as the water table, which separates saturated and unsaturated zones within geologic strata. In unconfined aquifers, the capillary rise may form a band of saturated sediment above the water table. This region is also known as a zone of tension saturation because tension forces pull the water upward into available pores, resulting in water pressures below atmospheric values in this zone. The capillary rise can extend above the water table from a few centimeters in sediments with large pores (e.g., clean gravel), up to several meters (e.g., 4e5m) in clay soils with small pores. Because the position of the water table varies with time due to seasonal and decadal changes in the supply and movement of groundwater, a variably saturated zone also can be defined (Fig. 1.1).

Drivers of groundwater flow The water content of the aquifer differs from the water flow, which is related to spatial gradients in the energy head. Water moves from high to low energy-head locations modulated by a conductivity coefficient describing the ease with which a given porous media transmits fluids. This phenomenon is described by Darcy’s (1856) law q ¼ K

dhT dl

(1.1)

where q is the flow per unit area (with dimensions of length, L, divided by time, T; L/T), K is the hydraulic conductivity (L/T), hT is the total energy head defined as the sum of the hydraulic pressure head hp, the elevation head hz (gravitational potential energy arising from elevation), and the velocity head hv (kinetic energy of the fluid velocity), all of which are expressed as the height of water (L), and l is the distance (L) over which the change in hT is evaluated. Because interstitial flows through porous media tend to be slow, hv is typically I. Setting the scene: groundwater as ecosystems

6

1. Hydrodynamics and geomorphology of groundwater environments

FIGURE 1.1 Cross-section of an aquifer. Blue lines with arrows show groundwater flow paths. Black diagonal lines portray main fractures.

negligible, such that hT is defined by the piezometric head hp þ hz, which is simply the elevation of the water table measured by subtracting the depth to groundwater from the land surface. Consequently, it is the higher altitude of the water table within a landscape that creates groundwater motion, just like in a closed U-shaped tube with a difference in water level that is suddenly opened. Groundwater motion may be conceptually defined as successive flow lines that act as separate tubes (Fig. 1.1). Figure 1.1 presents a cross-sectional view of a simple aquifer fully open to the atmosphere (unconfined aquifer), in which groundwater moves according to Darcy’s law from the mountain top toward the river valley along three nested flow paths in the variably saturated, permanently saturated, and fractured zones, respectively. The variably saturated zone represents the seasonal variation of the water table due to competition between recharge and depletion of the aquifer. Recharge is mainly driven by precipitation percolating into the soil, but is modulated by vegetation. When precipitation infiltrates the soil, some water that is held against gravity in pores due to matric forces (i.e., adhesion of water to solid surfaces and the attraction of water molecules to one another) is accessible by plants and can be removed via evapotranspiration from this near-surface water reservoir. Particularly in summer and spring, plant demand progressively depletes the soil water content. Once the soil water content increases and gravitational forces exceed matric forces, water flows through the soil and the unsaturated zone down to the water table and into the aquifer. Over geologic time, the water within the aquifer weathers the bedrock to a certain depth, below which groundwater moves more slowly through fissures and fractures in the more competent (less weathered)

I. Setting the scene: groundwater as ecosystems

The aquifer concept

7

parent bedrock (fractured zone). The rate of water movement (and thus its age) differs between the variably saturated, permanently saturated, and fractured (unweathered) zones due to differences in energy head, hydraulic conductivity, and the length of a given flow path (Fig. 1.1). Aquifers may also be encountered below geological formations at depths of several hundred meters, particularly in sedimentary basins. Such geological formations also have limited zones of water inflow (recharge zones) and present extremely slow renewal rates. Although present at great depths, these aquifers represent active microbial ecosystems (e.g., Chapelle, 2001). The outflow of these systems also supports oases and specific groundwater-dependent ecosystems. Closer to the surface, aquifers may not be entirely open to the atmosphere, covered by clay-rich (low permeability) layers or geologic formations that cap and confine the aquifer. Confined aquifers can exhibit substantially different geochemical compositions and limited fluxes of nutrients, thus representing a different ecosystem within the aquifer compared to unconfined strata. When aquifers are located at a great depth or close to a magmatic chamber in volcanic areas, temperature also becomes a driver of water motion and leads to the uprising and outflow of deep hot water (for example, geysers and geothermal vents). Indeed, volcanic areas are also the location of numerous thermal springs, which represent the outflow of hydrothermal convection cells. Thermal springs are frequent along mountain ranges, which induce large and deep hydrogeological loops of groundwater motion. In the deeper part of the loops, water encounters high temperatures and the upward movement of water is related to combined effects of thermal and head gradients. Such regional loops can also be present in nonmountainous areas, potentially with slight temperature anomalies (Fig. 1.2). This kind of hydrogeological situation is interesting as it induces mixing between deep and shallow groundwater with extremely different chemical compositions and biodiversity.

Aquifer hydrodynamics Porosity The total volume Vt (L3) of an aquifer can be divided into the volume of solids Vs and the volume of voids Vv. The ratio of Vv to Vt defines the porosity n (dimensionless) of the material, which is typically expressed as a percentage. There are several methods for determining porosity (Hao et al., 2008; Flint and Flint, 2018). Most commonly, it is determined by measuring the bulk density of the material and particle density of the solids. Other methods include obtaining a water-saturated sample of known volume and drying it in a laboratory oven (105 C). The difference in weight before and after drying (correcting for the temperature dependence of water density) gives information about the volume of water per total volume of the sample. For samples containing water that cannot be removed in a drying oven at those temperatures, the porosity can also be determined by sealing a sample of known volume with paraffin, placing it into the water, and measuring the displaced volume of water. The porosity gives the entire volume of the pore space, and thus gives information about the water volume potentially stored in an aquifer. However, a certain amount of pore space may contain entrapped air, rather than water, nor will all pores contribute to water flow due to, for example, dead-end pores, nonconnected pores, adhesively bound water, or hydrated water

I. Setting the scene: groundwater as ecosystems

8

1. Hydrodynamics and geomorphology of groundwater environments

FIGURE 1.2

Different levels of mixing in aquifers. Redrawn with permission from Fig. 1.14 of Roques (2013).

of clay minerals. When considering only the amount of void volume contributing to the water flow, the volume ratio is denoted as an effective porosity neff. In addition, there is a distinction between primary porosity (i.e., that of the deposited sediment or parent rock material) and secondary porosity (i.e., that due to subsequent chemical or physical weathering). The latter is of particular importance in the weathered and fractured zones of bedrock aquifers, as well as in karst aquifers. The value of porosity for unconsolidated material generally ranges from 25% to 70% (Freeze and Cherry, 1979) and is largely dependent on the size and shape of individual particles, and how well-sorted or uniform they are. Clay has higher porosity compared to sand or gravel, but is less permeable. For consolidated material, porosity values range from 0% to 50% (Freeze and Cherry, 1979) and are lower for crystalline rock or shale compared to fractured or karstic aquifers. When considering aquifers as habitat for organisms, the overall porosity is less important than the size of individual pores and the connectivity of the pore network. The pore size distribution defines whether aquifers are suitable habitats for biota, because they are restricted from actively moving or being transported through pores smaller than their own size (Fig. 1.3). Groundwater fauna is therefore mainly found in alluvial sediments with larger pores or in fractures or channels of fractured rocks or karst aquifers (Humphreys, 2009). However, it was found that some of these organisms not only use open voids, but are capable of modifying their environment by moving grains and digging through

I. Setting the scene: groundwater as ecosystems

The aquifer concept

9

FIGURE 1.3

Pore size classes (fine, medium, and large) as a function of different types of unconsolidated material (clay, silt, sand, and gravel) in comparison with size ranges for viruses, bacteria, protozoa, and fauna in aquifers. Modified with permission from Krauss and Griebler (2011) and Matthess and Pekdeger (1981), with fauna data from Stein et al. (2012) and Thulin and Hahn (2008).

porous sediment (Stumpp and Hose, 2017; Hose and Stumpp, 2019) or by moving into clay sediment (Korbel et al., 2019). For bacteria and viruses, most pores in unconsolidated material are wide enough for them to either be dispersed in water or attached to solid surfaces (Fig. 1.3). Permeability and hydraulic conductivity The pore size distribution not only forms a habitat for biota, but also dictates how fast water flows through an aquifer for a given head gradient, as described by Darcy’s law (1). The velocity of groundwater moving through pores and fractures, in turn, influences the energy needed for an organism to forage and live in such environments. The smaller the pore, the larger the flow resistance and the slower the flux. For uniform material and a unit head gradient, the fluid movement is proportional to the square of the mean pore diameter (Fetter, 2001). The proportional factor between the head gradient and the water flux is defined by the hydraulic conductivity K in Eq. (1.1). It combines properties of the fluid (viscosity and density) and of the sediment/rock material. The inherent property of the porous medium alone is its permeability k (L2), which is mainly controlled by the size distribution of the voids. Therefore, unconsolidated fine materials like clay, glacial tills, or silt have smaller permeability values (1019e1013 m2) compared to coarser materials like sand and gravel (1013e107 m2) (Freeze and Cherry, 1979; Gleeson et al., 2011). For consolidated rocks, permeability is generally low (1020e1012 m2) due to low porosity, particularly in the absence of secondary porosity features (fractures, channels). If such features are present and augmented by weathering of the parent rock, permeability is larger (1015e109 m2) and depends on how well those features are connected (Worthington et al., 2016).

I. Setting the scene: groundwater as ecosystems

10

1. Hydrodynamics and geomorphology of groundwater environments

Permeability and connectivity of pores also may affect the bioenergetics of organisms in terms of nutrient availability and foraging distances. Typically, the permeability and the hydraulic conductivity of a given medium are spatially variable (heterogeneous) depending on the structure, competence, and composition of the sediments/rocks. This is referred to as continuous heterogeneity because it describes the spatial variability of hydraulic properties within a given facies (e.g., a mixture of sand and gravel) due to the connectivity of porosity and fissures, which differs from categorical heterogeneity that describes changes in hydraulic conductivity among different facies (e.g., sand vs. gravel bodies). Permeability and hydraulic conductivity are often vector properties, leading to different behavior in the horizontal versus vertical directions (anisotropy). Both heterogeneity and anisotropy make it difficult to accurately measure the hydraulic conductivity in a representative elementary volume (REV, a volume of sediment large enough to capture the intrinsic process variability, but small enough to avoid combining variability among sediment types). Pumping tests or any other methods for determining hydraulic conductivity quantify the effective hydraulic conductivity, a lumped property controlled by the sediment/rock features having the largest hydraulic conductivity. Nevertheless, such values provide bulk information about the environment of the well during the pumping test. For scaling hydraulic conductivity and connectivity of specific hydrogeological features, regionalization methods can be used (Renard and Allard, 2013).

Geologic types of aquifers The above discussion of groundwater flow lines within aquifers is idealized, describing conditions that might exist in relatively homogeneous material, where hydraulic conductivity does not change spatially. In reality, any porous media has morphological and chemical variations that cause spatial changes in hydraulic conductivity, such that aquifers are intrinsically heterogeneous, but the degree of heterogeneity may vary from low to high. Furthermore, the geologic and geomorphic history of the landscape can have a strong influence on aquifer properties and function, with heterogeneous aquifers common in both karstic and fractured bedrock terrains. Karstic aquifers are mainly carbonate rocks (e.g., limestone), which are progressively dissolved by carbon dioxide (CO2) contained in water that originates from the soil due to organic matter degradation (White, 2002). Karst landscapes constitute 12%e15% of the continental surface. They are characterized by various dissolution features within the strata, including shafts and sinkholes, some of which may be primary locations for the inflow of surface water to the aquifer drainage system. Sinking streams are also a major feature of karst geomorphology and have attracted substantial attention due to the dramatic and flashy nature of flow in this part of the system (i.e., rapid flooding and drainage). The unsaturated zone of karstic systems also differs from more homogenous aquifers, typically characterized by dissolution features that may create specific local porosity in the first few meters of the karst surface. This zone of intense dissolution is termed the epikarst and may constitute a near-surface reservoir for the karst system, where water stored in the epikarst slowly infiltrates and recharges the underlying aquifer (Aquilina et al., 2006; Williams, 2008). Karstic aquifers are characterized by a drainage system that traverses the entire carbonate formation from surface input to outflow, which may be characterized by a complex series of

I. Setting the scene: groundwater as ecosystems

The aquifer concept

11

springs or a single dominant channel that controls a large part of the system. The drainage system is spectacular as it constitutes cavities that can be explored not only from a hydrogeological point of view but also for recreation and tourism. Karst aquifers are also important groundwater ecosystems because they can support larger groundwater fauna, such as fish (e.g., Hancock et al., 2005). Within the main channels of the karst drainage system (typically large caves), water flow is extremely rapid and produces spectacular floods that are often described as major characteristics of karstic systems. These open water flows are highly sensitive to human activities. Although the main channels of karst systems are typically flashy, matrix water within the carbonate aquifer contributes to the flow during the entire hydrological year, supplying water to outflow springs even when there is no surface-driven flooding in the main channels. Within the karst matrix, the transit time of water (i.e., the length of time spent traversing a given flow path) is often much longer than that of the primary drainage system of caverns and carbonate tunnels, providing strong mixing between rapid and slow flows (Long and Putnam, 2004; Bailly-Comte et al., 2011; Palcsu et al., 2021). Higher hydraulic head during flood events can cause a substantial flux of matrix water (Screaton et al., 2004), making many karstic systems flashy by nature, although the water that is flushed out during floods may have residence-times greater than assumed from the rapid pressure response (Kattan, 1997; Katz et al., 2001; Stuart et al., 2010; Han et al., 2015). Fractured bedrock aquifers are also highly heterogeneous systems (Neuman, 2005). Hardrock geologies represent about one-third of the continental surface and their aquifers thus comprise major water resources in many countries. In these systems, water circulates within the discontinuities of the rock (e.g., faults, fractures, and fissures). In contrast, the bedrock matrix itself has extremely low porosity and permeability and does not constitute a major water reservoir. Groundwater flow paths in fractured systems follow energy head gradients as presented in Fig. 1.1, but with more complex flow lines due to the heterogeneity of the medium. The formation of aquifers in hard-rock geologies requires intensive weathering of the bedrock over geologic time. Thus, fractured aquifers are often described as a weathered layer a few tens of meters thick, overlying the more competent parent bedrock. The weathered layer typically has a high clay content and is characterized as a hydrologically capacitive stratum, susceptible to human activities (Dewandel et al., 2006; Ayraud et al., 2008). The fractured part of the aquifer represents the transmissive part of the system and is more protected from human activities due to its deeper depth. The interface between the weathered and fractured zones is referred to as the weathering front and is a particularly reactive layer that is more intensively fractured than the underlying bedrock. Both layers represent fundamentally different systems, with differing hydrogeological properties and chemical compositions. Indeed, they also represent quite different ecosystems, with different microbial communities (Maamar et al., 2015). Karstic and fractured systems present a high degree of heterogeneity between their lowpermeability matrix material (competent bedrock) and the highly permeable karst conduits or hard-rock fractures. However, heterogeneity is manifested by different features over scales that vary by several orders of magnitude (Fig. 1.4AeC). For example, large regional faults may be present over several tens of kilometers along the surface of the landscape that transition to more localized fault networks at depth, with lengths of tens of meters. At smaller scales, fissures and cracks constitute discontinuities around faults or mineral boundaries. At even smaller scales, microscopic cracks and discontinuities in minerals create porosity

I. Setting the scene: groundwater as ecosystems

12

1. Hydrodynamics and geomorphology of groundwater environments

FIGURE 1.4 Heterogeneity in aquifers. Panels (AeC) show successive scales of heterogeneity in a fractured aquifer, while panel (D) shows heterogeneity and hydrobiogeochemical functioning in peat.

within the rock. All scales of discontinuities contribute to the wholeewater content of the aquifer, but with different properties. Large faults or fault zones may allow substantial fluid flow that is relatively more rapid, while the microporosity may act as a fluid reservoir. This affects both the hydrologic and chemical properties of the system. Even within relatively homogeneous aquifers, heterogeneity is also the rule, rather than the exception. Sandy aquifers contain both clay-rich and coarse facies that present local heterogeneity that respectively slows or accelerates water fluxes due to differences in grain size and hydraulic conductivity. These structures may also present distinct mineralogy and chemical reactivity. Heterogeneity is highly important for biogeochemical reactions and thus microbial ecosystems. Beyond the mean chemical characteristics of a given aquifer (e.g., chemical composition, pH, and redox), microsites within the aquifer may have very different conditions. For example, peatlands may be flushed by fresh water, resulting in overall oxic conditions, but intense sulfate reduction may occur in the microporosity of the peat, away from the main water flow (Fig. 1.4D). This allows resilience of peat and wetland systems that support relatively frequent water renewal while ensuring reducing functions such as denitrification (Racchetti et al., 2011).

I. Setting the scene: groundwater as ecosystems

Links to surface hydrology

13

Links to surface hydrology Aquifers are intimately linked to the surface hydrological system within watersheds. Rainfall and snowmelt percolate vertically through hillslope soils, helping to recharge the aquifer. However, most of this surface input moves laterally downslope and mainly supplies water to lakes and rivers in alluvial valleys (Fig. 1.1). The sediment in alluvial valleys is typically porous, allowing continued connection with the aquifer as the surface water flows down valley toward an ocean or terminal lake (endorheic or sink basin). Where the water table of the aquifer coincides with the water surface of rivers, subsurface flow is directed toward the river, since it represents the local topographic low point (Fig. 1.1). However, if the river flow is perched above the aquifer’s water table, the river water will be driven into the streambed, recharging the aquifer through percolation and vertical head gradients; in extreme cases, rivers may become seasonally dry, disappearing into their streambeds (ephemeral streams). These two conditions, in which the river either receives groundwater or contributes river flow to the aquifer, are referred to as gaining versus losing conditions, respectively. Such phenomena may vary seasonally as the water table of the aquifer rises or falls (Fig. 1.1), and the process applies to any surface water body (i.e., rivers, lakes, and wetlands). These conditions can also vary with climate, such that water bodies in humid regions are typically gaining, while those in arid regions are frequently losing. Water bodies in karst terrain are typically losing systems, with surface water descending into the aquifer through a variety of surface fractures/inlets (e.g., sinkholes/swallets, ponors, and shafts) (e.g., Monroe, 1970; Taylor and Greene, 2008). Because of the porous nature of alluvial sediments, the entire alluvial valley can be connected to the aquifer. For example, when rivers spill onto the valley floor during floods, water may pond for extensive periods of time, with some of this water percolating into the alluvial sediment and recharging the aquifer. Conversely, head gradients may cause the aquifer to direct water onto the floodplain via springs and seeps, which typically occur at the break in slope between hillslopes and the river valley or at topographic lows in the floodplain. Processes and rates of exchange between surface water and groundwater also may be influenced by geologic and geomorphic history in terms of how rugged the landscape is (topographic gradients) and the nature and stratigraphy of the bedrock geology and alluvial deposits. For example, volcanic eruptions can fill valleys with lava or ash, both of which have very different porosity and hydraulic conductivities. Similarly, glaciers create broad U-shaped valleys filled with sediments ranging from boulders to fine clay, resulting in different boundary conditions than valleys formed by faulting in the absence of glaciation. Extensive glacial advance can also erase topography and reorganize the direction and magnitude of surface runoff that occurs in river networks. Finally, human activity in river corridors (e.g., dams, diversions, levees, groundwater pumping, agriculture) can alter both surface and subsurface hydrological cycles and, in the long term, may significantly deplete aquifer resources and alter surface and subsurface ecosystems. Another important linkage between surface and subsurface water occurs through hyporheic exchange, which is the movement of river water into and out of the alluvium within the river valley over relatively short time frames and short flow paths compared to deep groundwater movement in the aquifer (Fig. 1.5). This cycling of river water into and out of the alluvium

I. Setting the scene: groundwater as ecosystems

14

1. Hydrodynamics and geomorphology of groundwater environments

FIGURE 1.5 Five scales of nested flow and exchange between surface and subsurface water for a longitudinal profile along a river valley: (A) microscale circulation (flow paths less than a channel width (W) in length) caused by local head variations at the streambed induced by objects in the flow (e.g., large particles, logs, and biotic mounds, such as salmon redds or root boles); (B) channel-unit scale due to streambed head variations around individual bed forms (e.g., dunes, bars, steps) or biotic structures (e.g., beaver dams, log jams), with flow paths up to several W; (C) channelreach scale due to streambed head variations across a sequence of similar channel units (e.g., pool-riffle morphology sensu Montgomery & Buffington, 1997), with flow paths of tens of W; (D) valley-segment scale driven by head variations from spatial changes in valley confinement (floodplain width), alluvial depth, or underlying bedrock topography, with flow paths of hundreds to thousands of W (Edwards, 1998; Baxter and Hauer, 2000; Dent et al., 2001; Malard et al., 2002); and (E) regional groundwater scale driven by head gradients due to overall basin slope and watertable slope, with flow paths >103 W. Horizontally shaded lenses are impervious clay layers that can alter the extent and direction of hyporheic exchange. Modified from Alley et al. (1999) and Buffington and Tonina (2009b).

allows mixing with the shallow groundwater, creating physical and biological gradients that structure both surface and subsurface ecosystems, creating complex biogeochemical cycles (Krause et al., 2011). Hyporheic exchange is driven by Darcy’s law (1), but the energy head is controlled by conditions within the stream and, in particular, at the streambed surface. As such, the velocity head is no longer negligible when considering hyporheic flow. In alluvial valleys, surface water and groundwater interact at different spatial and temporal scales that manifest as a hierarchy of nested circulation cells from near-surface hyporheic exchange to deep, regional, groundwater flow (Fig. 1.5). These scales are primarily formed because of different spatial patterns of energy head, some of which may vary temporally

I. Setting the scene: groundwater as ecosystems

Links to surface hydrology

15

(Tóth, 1963; Boano et al., 2014). Although each scale is idealized as a separate flow path, physical and chemical mixing between circulation cells occurs through numerous processes, including diffusion, advection, dispersion, divergence around heterogeneities of various scales (such as sand and clay lenses), and convergence in upwelling zones (Fig. 1.5). At the regional scale, groundwater flow depends on (1) the overall water-table slope, (2) water levels in surface water bodies (e.g., rivers, lakes, and wetlands), and (3) characteristics of the porous media (thickness, hydraulic conductivity, heterogeneity) (Winter et al., 1998). At this scale, the water table typically follows topographic relief, but in a subdued way (Tóth, 1963; Wörman et al., 2006), and the river network can be modeled as a series of straight line segments, with energy head varying over length scales of several thousand channel widths (Guevara Ochoa et al., 2020). The water-surface elevation of other water bodies, such as lakes and wetlands, can be treated as constant or varying temporally. Groundwater flow is constrained and modulated by geological features as discussed above. Local perturbations of the energy head (for instance due to a single groundwater pumping well) may have negligible impacts at this scale. Streams can be divided into losing, gaining, or neutral segments. As the spatial scale becomes smaller, topographic features within the river corridor become progressively more important. At the valley scale, circulation cells are driven not only by head gradients but by spatial changes in alluvial volume and hydraulic conductivity, which can be quantified by expanding the Darcy equation to account for spatial variation of those factors (Tonina and Buffington, 2009b). In particular, valley-scale circulation results from spatial changes in valley confinement (floodplain width), valley slope, geology (rock type), or underlying bedrock topography. Important features are bedrock knickpoints (Wondzell and Swanson, 1996, 1999; Baxter and Hauer, 2000) and large-scale changes in lithology and heterogeneity of alluvial deposits. For example, the frequency of elevation changes in the underlying bedrock topography may structure broad-scale variations in the depth of alluvium that in turn generate valley-scale circulation, with benthic animals congregating at upwelling locations due to relatively stable thermal and discharge regimes (Baxter and Hauer, 2000), although other physical factors may also influence habitat selection (Bean et al., 2014). Furthermore, at this scale, river hydraulics strongly influence the local connectivity between the river and its aquifer via relatively deep hyporheic exchange (Fig. 1.5). Rivers may now be modeled as a curvilinear bend moving through the floodplain, with changes in water-surface elevation and energy head dependent on spatial changes in channel roughness and geometry that can be predicted from one-dimensional hydraulic models (Fleckenstein et al., 2006; Lautz and Siegel, 2006). Sediment transport history also becomes important as buried paleochannels and stratigraphy of the streambed may form preferential hyporheic flow paths within the river valley (Stanford and Ward, 1993). At the channel-reach scale, the river appears as a collection of repeating sequences of channel units (e.g., step-pool or pool-riffle couplets) (Fig. 1.5), with head gradients structured by the amplitude and wavelength of bed topography, and spatial changes in river depth and slope (Elliott and Brooks, 1997a,b; Kasahara and Wondzell, 2003; Buffington and Tonina, 2009). Hyporheic circulation at this scale is shallower than that of valley-segment scales

I. Setting the scene: groundwater as ecosystems

16

1. Hydrodynamics and geomorphology of groundwater environments

but can be influenced by similar processes occurring at more local scales. These processes include changes in reach slope, mesoscale changes in the volume of alluvium, cross-valley head differences between the main channel and secondary channels (Kasahara and Wondzell, 2003), and flow through the floodplain (between meander bends (Wroblicky et al., 1998; Cardenas, 2009; Boano et al., 2010) or within buried paleochannels (Stanford and Ward, 1993). Reach-scale hyporheic circulation is also caused by irregularity amongst bed forms, with topographic low points driving larger-scale circulation and capturing hyporheic circulation of upstream channel units (Gooseff et al., 2006). Three-dimensional modeling of groundwater-surface water interaction at this scale may require two-dimensional hydraulic models of water-surface elevations within the stream to properly define both lateral and longitudinal gradients (Benjankar et al., 2016), but constant values also have been used (Storey et al., 2003). At channel-unit and micro scales, hyporheic circulation is shallow and completely enveloped within larger-scale boundary conditions, because the physical domain is not large enough for interstitial flows to adjust to the local pore conditions, but instead is fully dominated by the boundary conditions (Tonina et al., 2016). Channel-unit circulation is associated with head variations around individual morphologic elements, such as pools and bars (Zarnetske et al., 2011), or biotic structures, such as beaver dams and log jams. In contrast, microscale circulation results from local, small-scale variations in channel characteristics (e.g., variation of the head around individual logs or clusters of streambed particles, or variation of hydraulic conductivity around a buried sand lens within otherwise coarse alluvium). At this scale, nesting and foraging activity of benthic animals also can alter bed topography, grain size, and porosity, thereby inducing and modulating hyporheic circulation (Ziebis et al., 1996; Statzner et al., 1999; Tonina and Buffington, 2009a; Pledger et al., 2017; Sansom et al., 2018). Similarly, aquatic and riparian vegetation can cause hydraulic pressure variations that drive hyporheic circulation and fine-sediment deposition that alters hydraulic conductivity (e.g., Magliozzi et al., 2018). At the microscale, pressure and velocity fluctuations due to turbulence may cause mass exchange between the river flow and near-surface pore water, resulting in hyporheic exchange (Blois et al., 2014; Roche et al., 2019). Because turbulence rapidly decreases within sediment interstices, turbulence exchange is generally limited to a near-surface layer, with thicknesses ranging from 2 to 10 times the median grain size of the streambed sediment (Packman et al., 2004; Detert et al., 2007; Tonina and Buffington, 2007). The turbulence-damping effect of the sediment increases with fine sediment, such that sand-bed streams may have shallow depths of turbulence-induced hyporheic exchange compared to gravel-bed rivers. However, sand-bed rivers are characterized by migrating bedforms at most discharges (Mohrig and Smith, 1996), with bed load transport causing a plugflow mechanism of hyporheic exchange, known as turn-over (Elliott and Brooks, 1997a,b), in which surface water is trapped within sediment pores during bedform deposition, and released during erosion as the bedform migrates downstream. Consequently, the larger the bedform the deeper the exchange; similarly, the more active the bed load transport the faster the exchange. This mechanism may also occur in braided gravel-bed rivers due to their high rates of movement but is not expected to be important in other coarse-grained rivers, where bedforms are generally immobile except during bankfull flow or larger floods (Montgomery and Buffington, 1997).

I. Setting the scene: groundwater as ecosystems

Aquifer function

17

Aquifer function Flow and transport in aquifers Streamlines in a fluid flow as described earlier indicate the main flow direction/path. Mixing of water from different flow paths occurs where those lines converge; for example, at groundwater discharge locations, such as wetlands, springs, and in the vicinity of a well when water is pumped. In addition, temporal variability of mixing processes may occur. For example, seasonality in groundwater recharge causes variability in the mixing of different water from the unsaturated and saturated zone throughout the year (Jasechko et al., 2014). Mixing water from different flow paths can be particularly relevant for geochemical and ecological processes. Water from individual flow paths may have distinct physical, chemical, and biological compositions. When different types of water with different physical and chemical compositions mix, other reactions might be triggered as well. Those mixing processes can create hot spots and hot moments, where reaction rates are larger compared to surrounding locations or to other time periods (McClain et al., 2003). Mixing is also relevant when pumping a fully screened well, as water from very different flow lines converges at the well (Tonina and Bellin, 2008). Thus, any water sampled at such locations represents the weighted average of fluxes contributing to the sample, which may have a different biogeochemical composition than would otherwise occur at that location in the absence of mixing. For understanding the physical, chemical, and biological composition of groundwater, general transport processes are important in terms of how they influence the fate of reactive and nonreactive solutes or particles in groundwater. The general transport processes are advection, hydrodynamic dispersion, and diffusion. This applies to both reactive and nonreactive species, with the former also being affected by chemical reactions: dissolution, precipitation, and sorption. Advection is the entrainment of solutes/particles by the groundwater flux along flow paths. In contrast, hydrodynamic dispersion considers the entire distribution of fluid velocities within emicroscopically and macroscopically- nonuniform media and the consequent spreading of solutes in both the main flow direction (longitudinal dispersion) and perpendicular to it (transverse dispersion). The ability of a given media to disperse solutes is described in terms of its dispersivity, which is an empirical parameter that increases with scale and flow distance (Gelhar et al., 1992). Whereas hydrodynamic dispersion is a property of the flow field, and thus only relevant in a flowing system, diffusion results in the movement of solutes due to physical and chemical concentration gradients independent of fluid velocity. Because hydrodynamic dispersion and diffusion are often difficult to distinguish, their effects are often combined when modeling solute transport. Spreading due to diffusion becomes more important if fluid velocities are small and/or in the presence of immobile/stagnant water (Knorr and Blodau, 2009). Special behavior is shown by biporous systems, exhibiting large contrasts in permeability. Here, the transport of water is different from solutes, because the solutes diffuse from areas of high permeability into less permeable areas (or vice versa as a function of the concentration gradient). This process is of particular importance when considering the transport of pollutants, as these zones can act as long-term stores. Both, hydrodynamic dispersion and diffusion can strongly influence ecosystem services like the degradation of contaminants as they

I. Setting the scene: groundwater as ecosystems

18

1. Hydrodynamics and geomorphology of groundwater environments

contribute to mass transfer, thus potentially causing mass transfer limitations at various scales (Meckenstock et al., 2015). The processes described above may be limited by pore size. If particulate matter, either abiotic or biotic (e.g., viruses, bacteria, or groundwater fauna), is larger than a given pore size (Fig. 1.3), the particles simply cannot be transported through the porous media. Therefore, the particulate matter is filtered by the pores and/or is only transported in pores that are larger than the particle size. The former results in the retardation of particulate matter that may clog pores and further reduce transport, while the latter causes accelerated transport through larger pores with faster flow velocity. Thus, the average particle velocity (only transported through the larger pores) may be faster than the average velocity of all water in the system (flow through the entire pore system). The main retardation process concerning reactive solutes or particles is sorption (i.e., their interaction with the solid phase due to chemical or physical processes). Sorption strongly depends on surface properties and/or properties of the reactant and surrounding water (e.g., ion strength). Sorption can be irreversible (attachment only) or reversible (attachment and detachment). Sorption is an important process for many nutrients and pollutants, but also for viruses and bacteria affecting their fate in groundwater (Tufenkji, 2007). Although pollutants might be immobilized for long periods due to sorption, this is only temporal retardation of transport, not the elimination of the pollutants. Complete elimination of pollutants occurs when they are sufficiently degraded; however, more toxic metabolites can be formed. Pollution can be particularly problematic in karst systems due to the rapid input of pollutants to the groundwater system via fissures, macropores, and tunnels, with relatively less filtration of particulate matter compared to granular porous media.

Groundwater age From the flow paths and transport properties along those paths, time scales of flow and transport can be assessed. Those time scales of flow and transport also influence ecosystem processes and water quality because the time since groundwater was recharged is relevant for biogeochemical processes (van der Velde et al., 2010), weathering of minerals (Maher, 2010), degradation of pollutants (Meckenstock et al., 2015), water availability in the critical zone (the area between the vegetation canopy and unweathered subsurface bedrock; Grant and Dietrich, 2017; Sprenger et al., 2019), renewal of groundwater (Jasechko, 2019; Moeck et al., 2020), and estimation of groundwater volume (Gleeson et al., 2011). Thus, those time scales are also used to assess both the intrinsic and specific vulnerability of groundwater bodies (Chatton et al., 2016; Wachniew et al., 2016; Jasechko et al., 2017). A particular concern for human use of aquifers is quantifying renewal times so that groundwater is not overpumped and depleted relative to the time needed to replenish the aquifer; which is a common problem for aquifers containing very old groundwater, indicative of low renewal rates (le Gal La Salle et al., 2001; Favreau et al., 2002; Gonçalvès et al., 2013; Gardner and Heilweil, 2014). Groundwater age is generally defined as the time elapsed since groundwater entered the subsurface (Bethke and Johnson, 2008). The mean water transit time, sometimes referred to as the turnover time, is defined as the ratio of the mobile water volume to the volumetric flow rate (Kreft and Zuber, 1978). It is the mean time between when water enters and leaves the

I. Setting the scene: groundwater as ecosystems

Aquifer function

19

system, also referred to as the residence time. As the mobile water volume is rarely known, tracers in combination with mathematical models are often used to determine the transit times (Maloszewski and Zuber, 1982). However, certain tracers only cover certain ranges of expected water ages (Newman et al., 2006; Suckow, 2014). Further, in the presence of immobile water or for nonideal conditions, the tracer transit time is different from the water transit time because the tracer diffuses into immobile zones and back, thus increasing its transit time relative to water flow (Maloszewski et al., 2004). This complication can be addressed through multi-tracer studies to better understand mixing processes, aquifer functioning, and groundwater age. Understanding groundwater age and system behavior may also require knowing the distribution of transit and residence times. For example, very different distributions can have similar mean values (Wachniew et al., 2016), creating problems of equifinality. As such, one may need to know the entire distribution of transit and residence times to determine how potential pollutants are diluted or if preferential flow is of relevance. The estimation of mean transit times and transit-time distributions in groundwater has been a challenge for decades; an issue that has been summarized in several different reviews (Suckow, 2014; Turnadge and Smerdon, 2014; McCallum et al., 2015; Cartwright et al., 2017; Jasechko, 2019; Sprenger et al., 2019). Groundwater ages range from days to weeks for near-surface flow in the variably saturated zone (Ayraud et al., 2008; Le Gal La Salle et al., 2012; Marçais et al., 2018) or during flood events, particularly in karstic systems (Delbart et al., 2014; Palcsu et al., 2021). Such low residence times may be quantified using a variety of tracers (e.g., anthropogenic gases, organic matter, tritium, stable isotopes, and dyes). Groundwater ages rapidly increase with depth, spanning several decades to hundreds of years for both unconfined and confined aquifers, while ages of millions of years have also been determined in sedimentary basins associated with marine environments (Gleeson et al., 2000). Saline and extremely old fluids were also discovered in deep crystalline formations, representing extremely slow regional flow (Bottomley et al., 1994; Aquilina et al., 1997; Greene et al., 2008; Bucher and Stober, 2010) that is controlled by microporosity (Fig. 1.3) (Waber and Smellie, 2008; Aquilina and Dreuzy, 2011; Aquilina et al., 2015). Radioactive or accumulative tracers (14C, 4He, 36Cl, 39Ar, 40Ar, 81 Kr, 129I) were used to characterize these old ages. Although relationships to surface and nutrient fluxes are extremely limited, these deep aquifers constitute ecosystems with specific microbial communities (Pedersen, 1997; Hallbeck and Pedersen, 2008).

Modeling aquifers Groundwater flow in aquifers is typically more complex than what is shown in Fig. 1.1. Complex aquifers require comprehensive definitions of the geologic features of each rock type within an aquifer to correctly parameterize spatial variation of hydraulic conductivity. However, the degree of heterogeneity and the morphologic distribution of different rock/sediment facies is usually unknown. Nevertheless, establishing a model of the aquifer remains a useful tool for analyzing factors such as groundwater flow patterns, human uses of the resource, and transport properties of nutrients and pollutants. Approaches for modeling groundwater can be broadly divided into spatially-distributed vs. lumped-parameter models. The former typically employs finite analyses, in which the aquifer is divided into small cells

I. Setting the scene: groundwater as ecosystems

20

1. Hydrodynamics and geomorphology of groundwater environments

with distributed hydrogeological properties (e.g., MODFLOW; Langevin et al., 2017). These properties allow the flow and transport of material, along with their spatial variation, to be computed. Numerous other models exist that allow implementation of various hydrological and chemical processes, as well as coupling between surface and subsurface systems (e.g., PLFOTRAN (Hammond et al., 2012) and HydroGeoSphere (Therrien et al., 2010). Because the spatial distribution of hydraulic properties within the aquifer is typically unknown, they can be characterized as stochastic variables, producing a number of possible realizations. This is especially important for solute transport, where the fate of the solute is studied using a Monte Carlo approach in which many different realizations of hydraulic properties are generated, from which the solute transport and associated transformations are then studied statistically. “Black box” or lumped-parameter models have also been used to determine simple characteristics, such as groundwater flow or mean residence time (Małoszewski and Zuber, 1985). The simplest one is the piston-flow model, which describes the aquifer as a “tube” (Fig. 1.6A). The simple interpretation of groundwater “age” (discussed in the previous section) refers to this type of model. A more representative lumped-parameter model is the exponential approach, which integrates an infinity of flow lines along a vertical axis, with an exponentially decreasing proportion of flow lines with depth and age (Fig. 1.6B). The third type of lumped-parameter model, which characterizes conditions often observed in natural environments, is the binary mixing model (Fig. 1.6C). This model considers mixing between two water bodies, a modern component (which may be young recharge water or relatively recent groundwater) and an older component (which might be defined as containing no chlorofluorocarbons (CFCs, used as a tracer) or simply as older than the modern component). A variety of models also have been developed for different scales of hyporheic exchange that elucidate different hydraulic environments and their consequences for fauna and water quality (further discussed by Tonina and Buffington, this volume). Although hyporheic and groundwater models employ similar mechanics related to Darcy’s law, the coupling of the two is frequently uneven. For example, some studies combine complex hyporheic models with simplified groundwater flow (e.g., Boano et al., 2008; Marzadri et al., 2016), while others use complex groundwater models with simplified hyporheic flow (e.g., Therrien et al., 2010) that do not fully capture the various scales of flow and interaction illustrated in Fig. 1.5 without using high-resolution topography and a fine-scale numerical mesh. Recent modeling approaches use artificial intelligence, such as machine learning or neural networks, which are particularly promising for investigating heterogeneous and complex aquifers.

FIGURE 1.6 Lumped parameter models of aquifers: (A) piston flow model, (B) exponential model, and (C) binary mixing model. Original drawing from Condate-Eau laboratory, used with permission. I. Setting the scene: groundwater as ecosystems

The chemical composition of groundwater

21

The chemical composition of groundwater Origin of chemical compounds in surface waters Groundwater derives its chemical composition initially from seawater through the integration of sea spray in vapor fluxes that give birth to clouds. Precipitation thus contains chemical elements that derive mainly from seawater. Seawater influence is maximized in coastal areas, with chloride (Cl) concentration (the major ion in seawater) ranging from 15 to 25 mg/L. A few kilometers inland, this concentration rapidly decreases toward > arccos qH;G ¼ 1
2
> < p p um um (3.3) s ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi >
 2 > > v v v u gw gw gw > m :q arccos þ vgw 1
2
H;L ¼ p p um um um ¼ KC lhm tanhðldb Þ

(3.4)

where qH;G and qH;L are the mean hyporheic fluxes for gaining and loosing reaches, respectively, and um is the maximum downwelling velocity. Analytical solutions of the above equations demonstrate that the groundwater underflow (horizontal) velocity, ugw, does not affect

I. Setting the scene: groundwater as ecosystems

Predicting hyporheic exchange

67

the magnitude of hyporheic exchange, but does influence its extent and residence time (Boano et al., 2008; Fox et al., 2014; Marzadri et al., 2016). However, the vertical component of groundwater flow, vgw, strongly impacts the hyporheic exchange, such that the hyporheic zone is fully suppressed for vgw > um in Eq. (3.3) (Marzadri et al., 2016). Predictions from these equations have been confirmed by flume experiments, which mimicked ambient groundwater flows (Fox et al., 2014). The residence time distribution R of hyporheic flow weighted over the downwelling flux across a dune can be estimated by the following implicit equation as a function of time, t, and sediment porosity, n, for the case of vgw ¼ 0
   2p db 2a cos R tanh 4p2 KC hm t l ¼ l2 n R

(3.5)

and semianalytical solutions, which account for ambient groundwater flow, are also available (Bottacin-Busolin and Marion, 2010; Marzadri et al., 2016). In all cases, a lognormal distribution provides a good approximation of R (Wörman et al., 2002; Marzadri et al., 2016), although it has been suggested that its accuracy is less reliable in describing the tail of the distribution (Haggerty et al., 2002; Cardenas, 2007) and other distributions have been proposed (Grant et al., 2020). The vertical depth of hyporheic exchange, dh, when not confined by a finite depth of alluvium, db, scales with bedform length, with dh w1 l (Wörman et al., 2002), and also depends on the Reynolds number calculated from the mean velocity at the bedform crest, D (Cardenas and Wilson, 2007b). The above results for two-dimensional dunes can be used to approximate those of three-dimensional dunes, especially at high Reynolds numbers (Chen et al., 2015, 2018). Typically, dunes are not stationary, but migrate at a downstream velocity, Ub, causing progressive turnover of the sediment, which simultaneously releases and entraps hyporheic fluid (Fig. 3.2D). The dimensionless turnover number is (Elliott and Brooks, 1997) Tover ¼

nUb
ugw um

(3.6)

and can be used to estimate the relative dominance of pumping exchange (Tover7) (Elliott and Brooks, 1997), where Ub is multiplied by sediment porosity, n, to create a pore-water velocity of the same type as the Darcy velocities ugw and um. For turnover exchange (Tover>7), the mean downwelling flux can be quantified as q¼

Y0 nUb l

(3.7)

The maximum dh for turnover exchange was originally suggested to be limited by the amplitude of the largest migrating dune (Elliott, 1990), such that rapid dune migration reduces the depth of hyporheic exchange, which scales with D, compared to the case of pumping exchange, where dh scales with l. Subsequently, it has been proposed that turnover is always impacted by pumping, which advectively moves solute from the well-mixed turnover

I. Setting the scene: groundwater as ecosystems

68

3. Physical and biogeochemical processes of hyporheic exchange in alluvial rivers

region to the subsurface sediment, effectively increasing the depth of hyporheic exchange (Packman and Brooks, 2001). The original Elliott and Brooks model has been expanded for unsteady surface discharge (Boano et al., 2007b; 2010b), for horizontally stratified streambeds having different hydraulic conductivity (Marion et al., 2008a), and for the effects of colloid deposition within the hyporheic zone (Packman et al., 2000; Ren and Packman, 2004b, 2007). In addition to these analytical solutions, numerical simulations also have been used by coupling surface and groundwater models in fluvial (Cardenas and Wilson, 2007a; Janssen et al., 2012) and marine (Cardenas et al., 2008) dunes. Dune morphology quickly adapts to the applied discharge as sand is typically mobile, even at low flows. This suggests that analysis of hyporheic exchange in sand-bed rivers should account for the dependence of dune size on discharge (Boano et al., 2013). For instance, dune height and length in equilibrium with the stream flow can be assumed equal to 0.167 and 6 times Y0, respectively (Yalin, 1964). Furthermore, sand-bed rivers can exhibit a broad range of bed topography that varies systematically with discharge and bed load transport rate, transitioning from plane-bed to ripples to dunes and antidunes (e.g., Middleton and Southard, 1984), creating complex spatiotemporal changes in hyporheic exchange. Most solutions for hyporheic flow through dunes have been quantified assuming that hydraulic conductivity, Kc, is homogenous (same value throughout the domain) and isotropic (same value in all directions). For such conditions, Kc can be estimated as a function of a reference grain size, for instance the median grain size d50 (m) (Salarashayeri and Siosemarde, 2012; Gomez-Velez et al., 2015), Kc ¼ 119:06d1:62 50

(3.8)

Homogeneous and isotropic Kc values yield regular, smoothly varying hyporheic flow paths. In contrast, sediment heterogeneity (i.e., spatially variable Kc) leads to a seemingly erratic distribution of the interstitial flow field (Hester et al., 2013) and generates hyporheic exchange fluxes due to conservation of mass, causing the velocity and direction of subsurface flow to diverge due to spatial changes in sediment porosity (Vaux, 1968; Ward et al., 2011). The phenomenon can manifest at two distinct scales: (1) that of a single textural facies (continuous heterogeneity) (Hester et al., 2013), which is the intrinsic heterogeneity of a given porous material (e.g., sand) due to random spatial changes in grain size and porosity within a given medium and (2) that of multiple, juxtaposing, textural facies at larger spatial scales (categorical heterogeneity) (Winter and Tartakovsky, 2002; Riva et al., 2006; Pryshlak et al., 2015), forming a composite porous medium (e.g., sand and gravel layers, interspersed with clay lenses). Recent investigations for typical degrees of continuous heterogeneity of hydraulic conductivity in sand-bed streams (standard deviation of the log transformed Kc, i.e., s2Y < 0.6, where Y ¼ ln(Kc)), show that hyporheic exchange statistics at the bedform scale (e.g., residence time and mean fluxes) can be reasonably approximated using homogeneous Kc values (Tonina et al., 2016). Heterogeneity causes the hyporheic zone to be compressed toward the stream-water interface and an increase in tortuosity of hyporheic flow lines. The former effect reduces the length of the long flow lines (and their residence times), while the latter effect increases the length (and thus the residence times) of the short flow lines with respect to the

I. Setting the scene: groundwater as ecosystems

Predicting hyporheic exchange

69

case of homogeneous hydraulic conductivity. Because the hyporheic zone is strongly dominated by boundary conditions, especially the pressure profile at the wateresediment interface, heterogeneity may reduce the ensemble means of the hyporheic flow (e.g., residence time and fluxes) (Tonina et al., 2016) or increase them (Laube et al., 2018), depending on surface morphodynamic conditions and the consequent pressure distribution at the watere sediment interface. Anisotropy tends to reduce the uncertainty around the ensemble value, namely the difference in flow paths among all the possible heterogeneous realizations of the Kc-field. Investigations of categorical heterogeneity (flow through multiple textural facies) show similar results of compression of the hyporheic zone, but in general report a net result of reducing the hyporheic residence time and increasing the hyporheic discharge with increasing heterogeneity of hydraulic conductivity (Sawyer and Cardenas, 2009; GomezVelez et al., 2014; Pryshlak et al., 2015; Laube et al., 2018). Modeling of hyporheic exchange in gravel-bed rivers having a pool-riffle morphology (e.g., Montgomery and Buffington 1997) is more complex than dunes because the bedforms are three-dimensional and may be fully (Marzadri et al., 2010; Trauth et al., 2013) or partially (Tonina and Buffington, 2007; Monofy and Boano, 2021) submerged. For the fully-submerged case, semianalytical models show that the mean and variance of the residence time distribution (mt and st, respectively) depend on streambed morphology and surface hydrology, such that (Marzadri et al., 2010) mt ¼ 1:39 Y0:6 ; R2 ¼ 0:96 mt ¼

lmt KC si Cz

0:89 ; R2 ¼ 0:91 s2 t ¼ 2:07 Y
2 l 2 s2 st ¼ t K C si C z

(3.9)

(3.10)

where m*t and s2 t are the dimensionless mean and variance of the residence time distribution, respectively, si is the streambed slope, and Cz is the dimensionless Chézy number
 1 Cz ¼ 6 þ 2:5 ln (3.11) 2:5 ds with ds (¼d50/Y0) being the relative submergence of the sediment. The full hyporheic residence time can be approximated from the mean and variance, assuming a lognormal distribution (Marzadri et al., 2010; Tonina and Buffington, 2011). Similarly, the spatially averaged downwelling flow is estimated as (Tonina, 2012) q ¼ 41:108 Y
0:732 ; R2 ¼ 0:96 q ¼

q KC C4z

I. Setting the scene: groundwater as ecosystems

(3.12)

70

3. Physical and biogeochemical processes of hyporheic exchange in alluvial rivers

Semiempirical relationships, which account for the role of ambient groundwater (both basal (vertical) and underflow (horizontal)) are also available for fully submerged poolriffle bedforms (Trauth et al., 2013). For the case of partially submerged bars in gravel pool-riffle channels, the prediction of hyporheic exchange is based on empirical regressions (Tonina and Buffington, 2011; Trauth et al., 2013; Huang and Chui, 2018; Monofy and Boano, 2021), using a set of dimensional numbers such as those suggested by Tonina and Buffington (2011). P01 ¼ Y 1

¼

rUY0 U D l ; P02 ¼ pffiffiffiffiffiffiffiffi; P03 ¼ ; P04 ¼ ; P05 ¼ si ; Y0 Y0 m gY0

(3.13)

pffiffiffiffi Y rU K Y U2 Y Y0 Y D Y db ; 2 ¼ pffiffiffiffi; 3 ¼ pffiffiffiffi; 4 ¼ si ; 5 ¼ ; 6 ¼ pffiffiffiffi; m l g K K K

(3.14)

where r is the fluid density, m is the dynamic fluid viscosity, and K is the sediment permeability. The hyporheic exchange depth, dh, and the mean, mt, and standard deviation, st, of the hyporheic residence time distribution are then quantified as ! 5 X  0 dh ¼ exp Ai ln Pi (3.15) Y0 i¼1 ! 6 Y  X mt U pffiffiffiffi ¼ exp Bi ln i K i¼1

(3.16)

! 6 Y  X st U 0 pffiffiffiffi ¼ exp Bi ln i K i¼1

(3.17)

and the regression coefficients are reported in Table 3.1. In contrast to dunes, pool-riffle sequences form at high flows near bankfull stage (e.g., Montgomery and Buffington, 1997, 1998), when gravel substrates are set in motion (Tubino, 1991). Thus, for applications with discharges lower than bankfull, the streambed morphology

TABLE 3.1

Empirically determined parameters for, Eqs. (3.15)e(3.17), respectively, as proposed by Tonina and Buffington (2011).

i

1

2

3

4

5

6

Mean hyporheic depth (3.15)

Ai

0.152


0.058


0.509

0.074

0.906

Mean hyporheic residence time (3.16)

Bi


0.682

0.387

1.619

0.314


1.339

0.407

Standard deviation of the hyporheic residence time (3.17)

B’i


0.533

0.652

1.369

0.098


1.066

0.456

I. Setting the scene: groundwater as ecosystems

Predicting hyporheic exchange

71

in pool-riffle channels can be assumed stationary, while surface hydraulics change with discharge. Bedform length and amplitude can be predicted from bankfull width, Wb, and 1.45 depth, Y0b, such that: l ¼ 6.5Wb, and D ¼ Y0b/(0.18d0.45 ), where b is the half-channel s b aspect ratio b ¼ Y0/(2W) and valid for 2 100 m), such as the upper Mississippi, biogeochemical reactions within the water column are the main source of N2O (Marzadri et al., 2020). Four physical causes have been suggested for the reduced importance of the hyporheic zone relative to instream processes in controlling biogeochemical reactions with increasing river size: (1) lower rates of exchange between surface and subsurface flows due to systematic decreases in hydraulic conductivity as one moves downslope from small streams with gravel beds (high permeability) to large rivers with sand and gravel mixtures or sand and silt substrates (low permeability); (2) the above reduction in exchange combined with systematic increases in surface discharge as watercourses become larger causes a smaller ratio of hyporheic-to-instream discharge (Wondzell, 2011), (3) lower reaction-rate constants within streambed sediments, potentially due to low interstitial velocities (Reeder et al., 2018b), and (4) increases in the density and diversity of microbial communities and biofilms in the water column (Liu et al., 2013; Reisinger et al., 2015) due to increases in suspended sediment, which provide the supportive matrix for these organisms (Xia et al., 2009). Numerical models at bedform and reach scales have highlighted the role of stream topography, stream flow, groundwater flow, and hyporheic fluxes in controlling biogeochemical reactions (Fig. 3.3). However, application of these models at river-network scales is unfeasible. Recent studies, rooted in the Lagrangian approach (Ocampo et al., 2006; Marzadri et al., 2012; Zarnetske et al., 2012; Hampton et al., 2020), suggest that biogeochemical processes may scale with the Damköhler number, Da, defined as the ratio between the characteristic time scales of fluid advection and biogeochemical transformation. At the scale of individual flowlines, the advective time is simply the travel time, s, of the fluid along the flowline (Marzadri et al., 2012). However, at bedform scales, hyporheic flow has a distribution of residence times, which can be indexed by the median value, s50, to describe overall response to the bedform. Thus, at bedform and reach scales, Da is defined as the ratio between the corresponding s50 and the time scale of a given biogeochemical process, slim, expressed as the inverse of the reaction rate constant, Kre Da ¼

s50 ¼ s50 Kre slim

(3.18)

This approach has been shown to be effective for nitrous oxide, N2O, emissions in streams, with potential extension to other biogeochemical reactions (Zarnetske et al., 2011; Marzadri et

I. Setting the scene: groundwater as ecosystems

76

3. Physical and biogeochemical processes of hyporheic exchange in alluvial rivers

Reach-scale dimensionless N2O fluxes, F*N2O, generated from the benthic (red) and combined benthicehyporheic (gray) zones of headwater streams (channel widths less than 10 m) with pool-riffle or dune morphologies as a function of Damköhler number, Da, where s50 is the median residence time of the hyporheic flow and Kre is the reaction rate constant of denitrification, defined as the uptake rate normalized by the mean flow depth of the channel. F*N2O is defined as the N2O flux per unit area scaled by the total in-stream flux of a given dissolved inorganic nitrogen species (NO-3 and NHþ 4 ). Data are from the Kalamazoo River (Michigan) (Beaulieu et al., 2008, 2009) and the second Lotic Intersite Nitrogen eXperiment (LINXII), which includes sites throughout the United States and Puerto Rico, spanning a broad range of land use, land cover, biomes, climatic zones, and channel morphologies (Mulholland et al., 2008). Following Mulholland et al.’s (2008) classification, reference streams had more than 85% native vegetation, while agricultural and urban streams drained watersheds with varying proportions of those landcover types, respectively. Modified from Marzadri et al. (2017).

FIGURE 3.4

al., 2012, 2022). In particular, analysis of data from headwater streams shows that the reachscale dimensionless flux of N2O, F*N2O, exhibits a power-law scaling with Da that is independent of land use, ecohydromorphology, or climate (Marzadri et al., 2017) (Fig. 3.4). The study showed that the production of N2O from the benthic layer (red curve in Fig. 3.4) was almost an order of magnitude smaller than that from the combined emissions of the benthic and hyporheic zones in these small streams (black curve in Fig. 3.4). The two empirical power laws were then applied to a set of more than 400 stream reaches worldwide, providing good predictive power (Marzadri et al., 2017). The above analyses also show that not only are reactant loads (or concentrations) important, but stream morphology and hydraulics can regulate the amount of products generated (Marzadri et al., 2014). This is probably due to the fact that hyporheic exchange depends on stream hydromorphology (e.g., Buffington and Tonina 2009), which, in turn, may specialize the distribution of microbial communities and functioning (Quick et al., 2016). For example, microbes having the nirS gene, associated with denitrifying enzymes, cluster at the interface between the aerobiceanaerobic zone, the position of which is controlled by both flow

I. Setting the scene: groundwater as ecosystems

Conclusion

77

hydraulics and biogeochemical reaction rates (cf. Fig. 3.2G and H). Overall, local-scale processes within the hyporheic zone, benthic zone, and surface water column may have important effects at the global scale, because they may regulate riverine production of N2O and, thus, should be accounted for in predicting the impact of anthropogenic activities on biogeochemical processes in riverine systems (e.g., Marzadri et al., 2021).

Conclusion Surface water of alluvial rivers ubiquitously flows into and out of the interstitial spaces of the surrounding alluvium, creating a highly connected riverine ecosystem that extends well beyond the visible surface flow of rivers (Poole et al., 2008; Hauer et al., 2016). The extent of these flows depends on local conditions across multiple scales, including bedsurface grain size and heterogeneity, presence of microroughness elements (e.g., logs, boulders, biotic mounds), morphological characteristics of the stream (e.g., meso-scale variation of bed topography, flow depth, width, velocity), reach- to valley-scale morphology (macroscale variation of bedform sequences, slope, confinement, and alluvial volume), associated geologic constraints, and the position of the groundwater table (Krause et al., 2022). These different scales of physical conditions and constraints form a hierarchy of nested hyporheic cells, with larger scales enveloping smaller ones (Baxter and Hauer, 2000; Malard et al., 2002; Poole et al., 2008; Buffington and Tonina, 2009; Stonedahl et al., 2013). As the size of hyporheic cells increases, so does the residence time of stream water traversing the hyporheic zone, while the average interstitial flow velocity is reduced because pressure gradients become smaller over longer distances between two points. The net result is a set of nested transient storage zones, where biogeochemical reactions transform reactive solutes, with resultant products upwelling into the surface streamflow. These physical and chemical gradients have important implications for water quality in both surface and pore waters. However, the importance of hyporheic exchange on surface water quality is expected to be stream-size dependent, because as stream size increases, the ratio between hyporheic discharge and surface discharge decreases (Wondzell, 2011), diluting hyporheic products within the surface water. The fading of the importance of hyporheic processes on surface water quality in larger rivers is still under investigation, but the hyporheic zone is expected to remain an important and key element of river corridors even in large rivers as it may provide localized thermal, chemical, and hydraulic refugia for aquatic species, particularly in upwelling zones (Baxter and Hauer, 2000; Malard et al., 2002; Stanford et al., 2005; see review by Wondzell, 2011). In addition, the hyporheic zone has become a key element in stream and river restoration (Hester and Gooseff, 2010; Ward et al., 2011; Herzog et al., 2016), particularly where engineering solutions are required to better design this environment. Overall, a broad range of investigations are exploring the impact of morphological and biological heterogeneities on hyporheic conditions and how hyporheic processes respond to dynamic changes of solutes (Marzadri et al., 2013b; Kaufman et al., 2017) and surface and groundwater hydraulics (Krause et al., 2022). Furthermore, local hyporheic processes are being upscaled to more broadly predict water quality within riverine systems at watershed and regional scales (e.g., to address nutrient removal

I. Setting the scene: groundwater as ecosystems

78

3. Physical and biogeochemical processes of hyporheic exchange in alluvial rivers

and greenhouse gas emissions) (Stewart et al. 2011; Gomez-Velez and Harvey, 2014; Marzadri et al., 2017, 2021). These investigations may be supported by novel methodologies (1) in the laboratory, e.g., non-invasive approaches like optical measurements (Cardenas et al., 2016; Reeder et al., 2018b) and image analysis coupled with refractive index matching, RIM, which allows mapping of the flow field through solid grains (Voermans et al., 2018; Moreto et al., 2022) with biological activities (Rubol et al., 2018) and (2) in the field, including optical measurements (Vieweg et al., 2013; Reeder et al., 2019) and improved data analysis (e.g., water temperature time series (van Kampen et al., 2022)) and (3) data assimilation and distribution via machine learning (Marzadri et al., 2021) and numerical simulations (Chowdhury et al., 2020; Shen et al., 2020; Yuan et al., 2021).

Acknowledgments We thank Annika Quick, William Jeff Reeder and Alessandra Marzadri for providing data and helping with Figs. 3.2e3.4. Data were collected and analyzed with support from NSF grants 1141690, 1141752, 1344661, 1344602 and IIA-1301792 D.T. acknowledges support from the USDA National Institute of Food and Agriculture, Hatch project 1012806. We thank F. Boano for constructive comments that improved this chapter.

References Alley, W.M., Reilly, T.E., Franke, O.L., 1999. Sustainability of Ground-Water Resources. US Geological Survey, Circular 1186, Denver, CO. Argerich, A., Haggerty, R., Martí, E., Sabater, F., Zarnetske, J., 2011. Quantification of metabolically active transient storage (MATS) in two reaches with contrasting transient storage and ecosystem respiration. Journal of Geophysical Research: Biogeosciences 116, G03034. Baxter, C.V., Hauer, F.R., 2000. Geomorphology, hyporheic exchange, and selection of spawning habitat by bull trout (Salvelinus confluentus). Canadian Journal of Fisheries and Aquatic Sciences 57 (7), 1470e1481. https://doi.org/ 10.1139/f00-056. Beaulieu, J.J., Arango, C.P., Hamilton, S.K., Tank, J.L., 2008. The production and emission of nitrous oxide from headwater streams in the Midwestern United States. Global Change Biology 14 (4), 878e894. https://doi.org/10.1111/ j.1365-2486.2007.01485.x. Beaulieu, J.J., Arango, C.P., Tank, J.L., 2009. The effects of season and agriculture on nitrous oxide production in headwater streams. Journal of Environment Quality 38 (2), 637e646. https://doi.org/10.2134/jeq2008.0003. Bencala, K.E., Walters, R.A., 1983. Simulation of solute transport in a mountain pool-and-riffle stream: a transient storage model. Water Resources Research 19 (3), 718e724. Blois, G., Best, J.L., Sambrook Smith, G.H., Hardy, R.J., 2014. Effect of bed permeability and hyporheic flow on turbulent flow over bed forms. Geophysical Research Letters 41 (18), 6435e6442. Boano, F., Camporeale, C., Revelli, R., 2010a. A linear model for the coupled surface-subsurface flow in a meandering stream. Water Resources Research 46, W07535. Boano, F., Camporeale, C., Revelli, R., Ridolfi, L., 2006. Sinuosity-driven hyporheic exchange in meandering rivers. Geophysical Research Letters 33, L18406. https://doi.org/10.1029/2006GL027630. Boano, F., Harvey, J.W., Marion, A., Packman, A.I., Revelli, R., Ridolfi, L., Wörman, A., 2014. Hyporheic flow and transport processes: mechanisms, models, and biogeochemical implications. Reviews of Geophysics 52 (4), 603e679. https://doi.org/10.1002/2012RG000417. Boano, F., Packman, A.I., Cortis, A., Revelli, R., Ridolfi, L., 2007a. A continuous time random walk approach to the stream transport of solutes. Water Resources Research 43, W10425. Boano, F., Poggi, D., Revelli, R., Ridolfi, L., 2009. Gravity-driven water exchange between streams and hyporheic zones. Geophysical Research Letters 36, L20402. Boano, F., Revelli, R., Ridolfi, L., 2007b. Bedform-induced hyporheic exchange with unsteady flows. Advances in Water Resources 30, 148e156.

I. Setting the scene: groundwater as ecosystems

References

79

Boano, F., Revelli, R., Ridolfi, L., 2008. Reduction of the hyporheic zone volume due to the stream-aquifer interaction. Geophysical Research Letters 35, L09401. Boano, F., Revelli, R., Ridolfi, L., 2010b. Effect of streamflow stochasticity on bedform-driven hyporheic exchange. Advances in Water Resources 33, 1367e1374. Boano, F., Revelli, R., Ridolfi, L., 2013. Modeling hyporheic exchange with unsteady stream discharge and bedform dynamics. Water Resources Research 49, 4089e4099. https://doi.org/10.1002/wrcr.20322. Bott, T.L., Kaplan, L.A., Kuserk, F.T., 1984. Benthic bacterial biomass supported by stream water dissolved organic matter. Microbial Ecology 10, 335e344. Bottacin-Busolin, A., Marion, A., 2010. Combined role of advective pumping and mechanical dispersion on time scales of bed formeinduced hyporheic exchange. Water Resources Research 46, W08518. https://doi.org/ 10.1029/2009WR008892. Bray, E.N., Dunne, T., 2017. Subsurface flow in lowland river gravel bars. Water Resources Research 53 (9), 7773e7797. Briggs, M.A., Lautz, L.K., Hare, D.K., González-Pinzón, R., 2013. Relating hyporheic fluxes, residence times, and redox-sensitive biogeochemical processes upstream of beaver dams. Freshwater Science 32 (2), 622e641. https://doi.org/10.1899/12-110.1. Briggs, M.A., Lautz, L.K., McKenzie, J.M., Gordon, R.P., Hare, D.K., 2012. Using high-resolution distributed temperature sensing to quantify spatial and temporal variability in vertical hyporheic flux. Water Resources Research 48, W02527. Buffington, J.M., Tonina, D., 2009. Hyporheic exchange in mountain rivers II: effects of channel morphology on mechanics, scales, and rates of exchange. Geography Compass 3 (3), 1038e1062. https://doi.org/10.1111/j.17498198.2009.00225.x. Cardenas, M.B., 2007. Potential contribution of topography-driven regional groundwater flow to fractal stream chemistry: residence time distribution analysis of Tóth flow. Geophysical Research Letters 34, L05403. Cardenas, M.B., 2009a. Stream-aquifer interactions and hyporheic exchange in gaining and losing sinuous streams. Water Resources Research 45, W06429. Cardenas, M.B., 2009b. A model for lateral hyporheic flow based on valley slope and channel sinuosity. Water Resources Research 45 (1), W01501. https://doi.org/10.1029/2008WR007442. Cardenas, M.B., Wilson, J.L., 2007a. Dunes, turbulent eddies, and interfacial exchange with permeable sediments. Water Resources Research 43, W08412. Cardenas, M.B., Wilson, J.L., 2007b. Exchange across a sedimentewater interface with ambient groundwater discharge. Journal of Hydrology 346, 69e80. Cardenas, M.B., Zlotnik, V.A., 2003. Three-dimensional model of modern channel bend deposits. Water Resources Research 39 (6), 1141. https://doi.org/10.1029/2002WR001383. Cardenas, M.B., Cook, P.L.M., Jiang, H., Traykovski, P., 2008. Constraining denitrification in permeable waveinfluenced marine sediment using linked hydrodynamic and biogeochemical modeling. Earth and Planetary Science Letters 275 (1e2), 127e137. Cardenas, M.B., Ford, A.E., Kaufman, M.H., Kessler, A.J., Cook, P.L.M., 2016. Hyporheic flow and dissolved oxygen distribution in fish nests: the effects of open channel velocity, permeability patterns, and groundwater upwelling. Journal of Geophysical Research: Biogeosciences 121, 3113e3130. Castro, N.M., Hornberger, G.M., 1991. Surface-subsurface water interaction in an alluviated mountain stream channel. Water Resources Research 27 (7), 1613e1621. Chen, X., Cardenas, M.B., Chen, L., 2015. Three-dimensional versus two-dimensional bed form-induced hyporheic exchange. Water Resources Research 51, 2923e2936. https://doi.org/10.1002/2014WR016848. Chen, X., Cardenas, M.B., Chen, L., 2018. Hyporheic exchange driven by three-dimensional sandy bed forms: sensitivity to and prediction from bed form geometry. Water Resources Research 54 (6), 4131e4149. https://doi.org/ 10.1029/2018WR022663. Choi, J., Harvey, J.W., Conklin, M.H., 2000. Characterizing multiple timescales of stream and storage zone interaction that affect solute fate and transport in streams. Water Resources Research 36 (6), 1511e1518. Chowdhury, R.S., Zarnetske, J.P., Phanikumar, M.S., Briggs, M.A., Day-Lewis, F.D., Singha, K., 2020. Formation criteria for hyporheic anoxic microzones: assessing interactions of hydraulics, nutrients, and biofilms. Water Resources Research 56 (3), e2019WR025971. https://doi.org/10.1029/2019WR025971.

I. Setting the scene: groundwater as ecosystems

80

3. Physical and biogeochemical processes of hyporheic exchange in alluvial rivers

Constantz, J., 2008. Heat as a tracer to determine streambed water exchanges. Water Resources Research 44, W00D10. Cooper, A.C., 1965. The effect of transported stream sediments on the survival of sockeye and pink salmon eggs and alevin. International Pacific Salmon Fisheries Commission Bulletin 18, New Westminster, BC, Canada. Cranswick, R.H., Cook, P.G., Lamontagne, S., 2014. Hyporheic zone exchange fluxes and residence times inferred from riverbed temperature and radon data. Journal of Hydrology 519, 1870e1881. https://doi.org/10.1016/ j.jhydrol.2014.09.059. Dai, Z., Ritzi, R.W., Dominic, D.F., Rubin, Y.N., 2003. Estimating spatial correlation structure for permeability in sediments with hierarchical organization. In: Mishra, S. (Ed.), Probabilistic Approaches to Groundwater Modeling Symposium 2003. American Society of Civil Engineers, New York, NY. Dent, C.L., Grimm, N.B., Fisher, S.G., 2001. Multiscale effects of surface-subsurface exchange on stream water nutrient concentrations. Journal of the North American Benthological Society 20 (2), 162e181. Drummond, J.D., Aubeneau, A., Packman, A.I., 2014. Stochastic modeling of fine particulate organic carbon dynamics in rivers. Water Resources Research 50 (5), 4341e4356. Dudunake, T., Tonina, D., Reeder, W.J., Monsalve, A., 2020. Local and reach-scale hyporheic flow response from boulder-induced geomorphic changes. Water Resources Research 56 (10). https://doi.org/10.1029/ 2020WR027719. Edwards, R.T., 1998. The hyporheic zone. In: Naiman, R.J., Bilby, R.E. (Eds.), River Ecology and Management: Lessons From the Pacific Coastal Ecoregion. Springer-Verlag, New York, NY, pp. 399e429. Elliott, A.H., 1990. Transfer of Solutes Into and Out of Streambeds, Rep. KH-R-52. W.M. Keck Laboratory of Hydraulics and Water Resources, California Institute of Technology, Pasadena, CA. Elliott, A.H., Brooks, N.H., 1997. Transfer of nonsorbing solutes to a streambed with bed forms: laboratory experiments. Water Resources Research 33 (1), 137e151. De Falco, N., Boano, F., Bogler, A., Bar-Zeev, E., Arnon, S., 2018. Influence of stream-subsurface exchange flux and bacterial biofilms on oxygen consumption under nutrient-rich conditions. Journal of Geophysical Research: Biogeosciences 123 (7), 2021e2034. Fanelli, R.M., Lautz, L.K., 2008. Patterns of water, heat and solute flux through streambeds around small dams. Ground Water 46 (5), 671e687. Findlay, S., Strayer, W., Goumbala, C., Gould, K., 1993. Metabolism of streamwater dissolved organic carbon in the shallow hyporheic zone. Limnology & Oceanography 38, 1493e1499. Fleckenstein, J.H., Niswonger, R.G., Fogg, G.E., 2006. River-aquifer interactions, geologic heterogeneity, and low-flow management. Ground Water 44, 837e852. Fox, A., Boano, F., Arnon, S., 2014. Impact of losing and gaining streamflow conditions on hyporheic exchange fluxes induced by dune-shaped bed forms. Water Resources Research 50, 1895e1907. Gariglio, F.P., Tonina, D., Luce, C.H., 2013. Spatio-temporal variability of hyporheic exchange through a pool-rifflepool sequence. Water Resources Research 49 (11), 7185e7204. https://doi.org/10.1002/wrcr.20419. Gibert, J., Stanford, J.A., Dole-Olivier, M.-J., Ward, J.V., 1994. Basic attributes of groundwater ecosystems and prospects for research. In: Gilbert, J., Danielpol, D.L., Standford, J.A. (Eds.), Groundwater Ecology. Academic Press, San Diego, CA, pp. 8e40. Gomez-Velez, J.D., Harvey, J.W., 2014. A hydrogeomorphic river network model predicts where and why hyporheic exchange is important in large basins. Geophysical Research Letters 41 (18), 6403e6412. https://doi.org/10.1002/ 2014GL061099. Gomez-Velez, J.D., Harvey, J.W., Cardenas, M.B., Kiel, B., 2015. Denitrification in the Mississippi River network controlled by flow through river bedforms. Nature Geoscience 8 (October), 1e8. https://doi.org/10.1038/ ngeo2567. Gomez-Velez, J.D., Krause, S., Wilson, J.L., 2014. Effect of low-permeability layers on spatial patterns of hyporheic exchange and groundwater upwelling. Water Resources Research 50, 5196e5215. González-Pinzón, R., Haggerty, R., Myrold, D.D., 2012. Measuring aerobic respiration in stream ecosystems using the resazurin-resorufin system. Journal of Geophysical Research 117, G00N06. Gooseff, M.N., 2010. Defining hyporheic zones- Advancing our conceptual and operational definitions of where stream water and groundwater meet. Geography Compass 4 (8), 945e955. Gooseff, M.N., McGlynn, B.L., 2005. A stream tracer technique employing ionic tracers and specific conductance data applied to the Maimai catchment, New Zealand. Hydrological Processes 19, 2491e2506. https://doi.org/ 10.1002/hyp.5685.

I. Setting the scene: groundwater as ecosystems

References

81

Gooseff, M.N., Anderson, J.K., Wondzell, S.M., LaNier, J., Haggerty, R., 2006. A modelling study of hyporheic exchange pattern and the sequence, size, and spacing of stream bedforms in mountain stream networks, Oregon, USA. Hydrological Processes 20 (11), 2443e2457. Gooseff, M.N., Hall, R.O.J., Tank, J.L., 2007. Relating transient storage to channel complexity in streams of varying land use in Jackson Hole, Wyoming. Water Resources Research 43, W01417. Grant, S.B., Gomez-Velez, J.D., Ghisalberti, M., 2018. Modeling the effects of turbulence on hyporheic exchange and local-to-global nutrient processing in streams. Water Resources Research 54 (9), 5883e5889. https://doi.org/ 10.1029/2018WR023078. Grant, S.B., Monofy, A., Boano, F., Gomez-Velez, J.D., Guymer, I., Harvey, J., Ghisalberti, M., 2020. Unifying advective and diffusive descriptions of bedform pumping in the benthic biolayer of streams. Water Resources Research 56 (11), e2020WR027967. https://doi.org/10.1029/2020WR027967. Haggerty, R., Wondzell, S.M., Johnson, M.A., 2002. Power-law residence time distribution in hyporheic zone of a 2nd-order mountain stream. Geophysical Research Letters 29 (13), 4. Haggerty, R., Reeves, P., 2002. STAMM-L Version 1.0 User’s Manual. Sandia National Laboratory, Albuquerque, NM. Haggerty, R., Martí, E., Argerich, A., von Schiller, D., Grimm, N.B., 2009. Resazurin as a “smart” tracer for quantifying metabolically active transient storage in stream ecosystems. Journal of Geophysical Research 114 (G3), G03014. https://doi.org/10.1029/2008JG000942. Harvey, A.M., Wagner, B.J., 2000. Quantifying hydrologic interactions between streams and their subsurface hyporheic zones. In: Jones, J.B., Mulholland, P.J. (Eds.), Streams and Ground Waters. Academic Press, San Diego, CA, pp. 3e44. Hampton, T.B., Zarnetske, J.P., Briggs, M.A., MahmoodPoor Dehkordy, F., Singha, K., Day-Lewis, F.D., Harvey, J.W., Chowdhury, S.R., Lane, J.W., 2020. Experimental shifts of hydrologic residence time in a sandy urban stream sedimentewater interface alter nitrate removal and nitrous oxide fluxes. Biogeochemistry 149 (2), 195e219. https://doi.org/10.1007/s10533-020-00674-7. Harvey, C., Gorelick, S.M., 2000. Rate-limited mass transfer or macrodispersion: which dominates plume evolution at the Macrodispersion Experiment (MADE) site? Water Resources Research 36 (3), 637e650. Harvey, J.W., Bencala, K.E., 1993. The effect of streambed topography on surface-subsurface water exchange in mountain catchments. Water Resources Research 29 (1), 89e98. https://doi.org/10.1029/92WR01960. Harvey, J.W., Böhlke, J.K., Voytek, A.M., Scott, D., Tobias, C.R., 2013. Hyporheic zone denitrification: controls on effective reaction depth and contribution to whole-stream mass balance. Water Resources Research 49 (10), 6298e6316. Harvey, J.W., Drummond, J.D., Martin, R.L., McPhillips, L.E., Packman, A.I., Jerolmack, D.J., Stonedahl, S.H., Aubeneau, A.F., Sawyer, A.H., Larsen, L.G., Tobias, C.R., 2012. Hydrogeomorphology of the hyporheic zone: stream solute and fine particle interactions with a dynamic streambed. Journal of Geophysical Research: Biogeosciences 117, G00N11. Harvey, J.W., Wagner, B.J., Bencala, K.E., 1996. Evaluating the reliability of the stream tracer approach to characterize stream-subsurface water exchange. Water Resources Research 32 (8), 2441e2451. Hassan, M.A., Tonina, D., Beckie, R.D., Kinnear, M., 2015. The effects of discharge and slope on hyporheic flow in step-pool morphologies. Hydrological Processes 29 (3), 419e433. https://doi.org/10.1002/hyp.10155. Hatch, C., Fisher, A.T., Revenaugh, J.S., Constantz, J., Ruehl, C., 2006. Quantifying surface wateregroundwater interactions using time series analysis of streambed thermal records: method development. Water Resources Research 42, W10410. Hauer, F.R., Locke, H., Dreitz, V.J., Hebblewhite, M., Lowe, W., Muhfeld, C., Nelson, C., Proctor, M., Rood, S., 2016. Gravel-bed river floodplains are the ecological nexus of glaciated mountain landscapes. Science Advances 2 (6), 2:e1600026. https://doi.org/10.1126/sciadv.1600026. Herzog, S.P., Higgins, C.P., McCray, J.E., 2016. Engineered streambeds for induced hyporheic flow: enhanced removal of nutrients, pathogens, and metals from urban streams. Journal of Environmental Engineering 142 (1), 1e10. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001012. Hester, E.T., Cardenas, M.B., Haggerty, R., Apte, S.V., 2017. The importance and challenge of hyporheic mixing. Water Resources Research 53 (5), 3565e3575. Hester, E.T., Doyle, M.W., 2008. In-stream geomorphic structures as drivers of hyporheic exchange. Water Resources Research 44 (3), W03417. https://doi.org/10.1029/2006WR005810.

I. Setting the scene: groundwater as ecosystems

82

3. Physical and biogeochemical processes of hyporheic exchange in alluvial rivers

Hester, E.T., Gooseff, M.N., 2010. Moving beyond the banks: hyporheic restoration is fundamental to restoring ecological services and functions of streams. Environmental Science and Technology 44 (5), 1521e1525. https://doi.org/10.1021/es902988n. Hester, E.T., Young, K.I., Widdowson, M.A., 2013. Mixing of surface and groundwater induced by riverbed dunes: implications for hyporheic zone definitions and pollutant reactions. Water Resources Research 49, 5221e5237. Huang, P., Chui, T.F.M., 2018. Empirical equations to predict the characteristics of hyporheic exchange in a pool-riffle sequence. Ground Water 56 (6), 947e958. https://doi.org/10.1111/gwat.12641. Hutchinson, P.A., Webster, I.T., 1998. Solute uptake in aquatic sediment due to current-obstacle interactions. Journal of Environmental Engineering 124 (5), 419e426. https://doi.org/10.1061/(ASCE)0733-9372(1998)124:5(419). Ikeda, S., 1984. Prediction of alternate bar wavelength and height. Journal of Hydraulic Engineering 110, 371e386. Janssen, F., Cardenas, M.B., Sawyer, A.H., Dammrich, T., Krietsch, J., Beer, D., 2012. A comparative experimental and multiphysics computational fluid dynamics study of coupled surfaceesubsurface flow in bed forms. Water Resources Research 48 (8), W08514. Janssen, F., Huettel, M., Witte, U., Faerber, P., Huettel, M., Meyer, V., Witte, U., 2005. Pore-water advection and solute fluxes in permeable marine sediments (I): calibration and performance of the novel benthic chamber system Sandy. Limnology & Oceanography 50 (3), 768e778. https://doi.org/10.4319/lo.2005.50.3.0779. Kaufman, M.H., Cardenas, M.B., Buttles, J., Kessler, A.J., Cook, P.L.M., 2017. Hyporheic hot moments: dissolved oxygen dynamics in the hyporheic zone in response to surface flow perturbations. Water Resources Research 53, 6642e6662. Kiel, B.A., Cardenas, M.B., 2014. Lateral hyporheic exchange throughout the Mississippi River network. Nature Geoscience 7 (6), 413e417. https://doi.org/10.1038/ngeo2157. Knapp, J.L.A., González-Pinzón, R., Drummond, J.D., Larsen, L.G., Cirpka, O.A., Harvey, J.W., 2017. Tracer-based characterization of hyporheic exchange and benthic biolayers in streams. Water Resources Research 53 (2), 1575e1594. https://doi.org/10.1002/2016WR019393. Krause, S., Abbott, B.W., Baranov, V., Bernal, S., Blaen, P., Datry, T., Drummond, J., Fleckenstein, J.H., Velez, J.G., Hannah, D.M., Knapp, J.L.A., Kurz, M., Lewandowski, J., Martí, E., Mendoza-Lera, C., Milner, A., Packman, A., Pinay, G., Ward, A.S., Zarnetzke, J.P., 2022. Organizational principles of hyporheic exchange flow and biogeochemical cycling in river networks across scales. Water Resources Research 58 (3), e2021WR029771. https://doi.org/10.1029/2021WR029771. Laube, G., Schmidt, C., Fleckenstein, J.H., 2018. The systematic effect of streambed conductivity heterogeneity on hyporheic flux and residence time. Advances in Water Resources 122, 60e69. https://doi.org/10.1016/ j.advwatres.2018.10.003. Lautz, L.K., Siegel, D.I., 2006. Modeling surface and ground water mixing in the hyporheic zone using MODFLOW and MT3D. Advances in Water Resources 29 (11), 1618e1633. Liu, T., Xia, X., Liu, S., Mou, X., Qiu, Y., 2013. Acceleration of denitrification in turbid rivers due to denitrification occurring on suspended sediment in oxic waters. Environmental Science and Technology 47 (9), 4053e4061. https://doi.org/10.1021/es304504m. Magliozzi, C., Grabowski, R.C., Packman, A.I., Krause, S., 2018. Toward a conceptual framework of hyporheic exchange across spatial scales. Hydrology and Earth System Sciences 22 (12), 6163e6185. https://doi.org/ 10.5194/hess-22-6163-2018. Malard, F., Tockner, K., Dole-Olivier, M.-J.J., Ward, J.V., 2002. A landscape perspective of surfaceesubsurface hydrological exchanges in river corridors. Freshwater Biology 47 (4), 621e640. https://doi.org/10.1046/j.13652427.2002.00906.x. Malcolm, I.A., Soulsby, C., Youngson, A.F., Hannah, D.M., 2005. Catchment-scale controls on groundwater-surface water interactions in the hyporheic zone: implications for salmon embryo survival. River Research and Applications 21, 977e989. Marion, A., Bellinello, M., Guymer, I., Packman, A.I., 2002. Effect of bed form geometry on the penetration of nonreactive solutes into a streambed. Water Resources Research 38 (10), 1209. Marion, A., Packman, A.I., Zaramella, M., Bottacin-Busolin, A., 2008a. Hyporheic flows in stratified beds. Water Resources Research 44, W09433. Marion, A., Zaramella, M., Bottacin-Busolin, A., 2008b. Solute transport in rivers with multiple storage zones: the STIR model. Water Resources Research 44, W10406.

I. Setting the scene: groundwater as ecosystems

References

83

Marzadri, A., Bellin, A., Tank, J.L., Tonina, D., 2022. Predicting nitrous oxide emissions through riverine networks. Science of The Total Environment 843, 156844. https://doi.org/10.1016/j.scitotenv.2022.156844. Marzadri, A., Dee, M.M., Tonina, D., Bellin, A., Tank, J.L., 2014. A hydrologic model demonstrates nitrous oxide emissions depend on streambed morphology. Geophysical Research Letters 41 (15), 5484e5491. https:// doi.org/10.1002/2014GL060732. Marzadri, A., Dee, M.M., Tonina, D., Bellin, A., Tank, J.L., 2017. Role of surface and subsurface processes in scaling N2O emissions along riverine networks. Proceedings of the National Academy of Sciences 114 (17), 4330e4335. https://doi.org/10.1073/pnas.1617454114. Marzadri, A., Tonina, D., Bellin, A., 2011. A semianalytical three-dimensional process-based model for hyporheic nitrogen dynamics in gravel bed rivers. Water Resources Research 47 (11), W11518. https://doi.org/10.1029/ 2011WR010583. Marzadri, A., Tonina, D., Bellin, A., 2012. Morphodynamic controls on redox conditions and on nitrogen dynamics within the hyporheic zone: application to gravel bed rivers with alternate-bar morphology. Journal of Geophysical Research: Biogeosciences 117 (3). https://doi.org/10.1029/2012JG001966. Marzadri, A., Tonina, D., Bellin, A., 2013a. Effects of stream morphodynamics on hyporheic zone thermal regime. Water Resources Research 49 (4), 2287e2302. https://doi.org/10.1002/wrcr.20199. Marzadri, A., Tonina, D., Bellin, A., 2013b. Quantifying the importance of daily stream water temperature fluctuations on the hyporheic thermal regime: implication for dissolved oxygen dynamics. Journal of Hydrology 507, 241e248. https://doi.org/10.1016/j.jhydrol.2013.10.030. Marzadri, A., Tonina, D., Bellin, A., 2020. Power law scaling model predicts N2O emissions along the Upper Mississippi River basin. Science of the Total Environment 732, 138390. https://doi.org/10.1016/j.scitotenv.2020.138390. Marzadri, A., Tonina, D., Bellin, A., Valli, A., 2016. Mixing interfaces, fluxes, residence times and redox conditions of the hyporheic zones induced by dune-like bedforms and ambient groundwater flow. Advances in Water Resources 88, 139e151. https://doi.org/10.1016/j.advwatres.2015.12.014. Marzadri, A., Tonina, D., Bellin, A., Vignoli, G., Tubino, M., 2010. Semianalytical analysis of hyporheic flow induced by alternate bars. Water Resources Research 46 (7), W07531. https://doi.org/10.1029/2009WR008285. Marzadri, A., Amatulli, G., Tonina, D., Bellin, A., Shen, L.Q., Allen, G.H., Raymond, P.A., 2021. Global riverine nitrous oxide emissions: the role of small streams and large rivers. Science of the Total Environment 776, 145148. https://doi.org/10.1016/j.scitotenv.2021.145148. Master, Y., Shavit, U., Shaviv, A., 2005. Modified isotope pairing technique to study N transformations in polluted aquatic systems: theory. Environmental Science and Technology 39, 1749e1756. Mendoza, C., Zhou, D., 1992. Effects of porous bed on turbulent stream flow above bed. Journal of Hydraulic Engineering 118 (9), 1222e1240. Middleton, G.V., Southard, J.B., 1984. Mechanics of Sediment Movement. Society for Economic Paleontologists and Mineralogists Short Course No. 3, Tulsa, OK. Monofy, A., Boano, F., 2021. The effect of streamflow, ambient groundwater, and sediment anisotropy on hyporheic zone characteristics in alternate bars. Water Resources Research 57, 1e22. https://doi.org/10.1029/ 2019WR025069. Montgomery, D.R., Buffington, J.M., 1997. Channel-reach morphology in mountain drainage basins. Geological Society of America Bulletin 109, 596e611. Montgomery, D.R., Buffington, J.M., 1998. Channel processes, classification, and response. In: Naiman, R.J., Bilby, R. (Eds.), River Ecology and Management. Springer-Verlag, New York, NY, pp. 13e42. Moreto, J.R., Reeder, W.J., Budwig, R., Tonina, D., Liu, X., 2022. Experimentally mapping water surface elevation, velocity, and pressure fields of an open channel flow around a stalk. Geophysical Research Letters 49 (7), 1e10. https://doi.org/10.1029/2021gl096835. Mrokowska, M.M., Osuch, M., 2011. Assessing validity of the dead zone model to characterize transport of contaminants in the River Wkra. In: Rowinski, P. (Ed.), Experimental Methods in Hydraulic Research, Geoplanet: Earth and Planetary Sciences, vol 1. Springer, Berlin, Heidelberg, pp. 235e246. Mulholland, P.J., Helton, A.M., Poole, G.C., Hall, R.O., Hamilton, S.K., Peterson, B.J., Tank, J.L., Ashkenas, L.R., Cooper, L.W., Dahm, C.N., et al., 2008. Stream denitrification across biomes and its response to anthropogenic nitrate loading. Nature 452 (7184), 202e205. https://doi.org/10.1038/nature06686.

I. Setting the scene: groundwater as ecosystems

84

3. Physical and biogeochemical processes of hyporheic exchange in alluvial rivers

Mulholland, P.J., Marzorf, E.R., Webster, J.R., Hart, D.D., Hendricks, S.P., 1997. Evidence that hyporheic zones increase heterotrophic metabolism and phosphorus uptake in forest streams. Limnology & Oceanography 42, 443e451. Naegeli, M.W., Uehlinger, U., 1997. Contribution of the hyporheic zone to ecosystem metabolism in a prealpine gravel-bed-river. Journal of the North American Benthological Society 16 (4), 794e804. Nagaoka, H., Ohgaki, S., 1990. Mass transfer mechanism in a porous riverbed. Water Research 24 (4), 417e425. Ocampo, C.J., Oldham, C.E., Sivapalan, M., 2006. Nitrate attenuation in agricultural catchments: shifting balances between transport and reaction. Water Resources Research 42 (W01408), 16. Orghidan, T., 1959. Ein neuer lebensraum des unterirdischen wassers: der hyporheische biotop. Archiv für Hydrobiologie 55, 392e414. Packman, A.I., Brooks, N.H., 2001. Hyporheic exchange of solutes and colloids with moving bed forms. Water Resources Research 37 (10), 2591e2605. https://doi.org/10.1029/2001WR000477. Packman, A.I., Brooks, N.H., Morgan, J.J., 2000. A physicochemical model for colloid exchange between a stream and a sand streambed with bed forms. Water Resources Research 36 (8), 2351e2361. Pescimoro, E., Boano, F., Sawyer, A.H., Soltanian, M.R., 2019. Modeling influence of sediment heterogeneity on nutrient cycling in streambeds. Water Resources Research 55 (5), 4082e4095. https://doi.org/10.1029/ 2018WR024221. Poole, G.C., O’Daniel, S.J., Jones, K.L., Woessner, W.W., Bernhardt, E.S., Helton, A.M., Stanford, J.A., Boer, B.R., Beechie, T.J., 2008. Hydrologic spiralling: the role of multiple interactive flow paths in stream ecosystems. River Research and Applications 24, 1018e1031. Pryshlak, T.T., Sawyer, A.H., Stonedahl, S.H., Soltanian, M.R., 2015. Multiscale hyporheic exchange through strongly heterogeneous sediments. Water Resources Research 51 (11), 9127e9140. Quick, A.M., Reeder, W.J., Farrell, T.B., Tonina, D., Feris, K.P., Benner, S.G., 2016. Controls on nitrous oxide emissions from the hyporheic zones of streams. Environmental Science and Technology 50 (21), 11491e11500. https:// doi.org/10.1021/acs.est.6b02680. Raymond, P.A., Zappa, C.J., Butman, D., Bott, T.L., Potter, J., Mulholland, P.J., Laursen, A.E., McDowell, W.H., Newbold, D., 2012. Scaling the gas transfer velocity and hydraulic geometry in streams and small rivers. Limnology & Oceanography 2 (1), 41e53. https://doi.org/10.1215/21573689-1597669. Reeder, W.J., Quick, A.M., Farrell, T.B., Benner, S.G., Feris, K.P., Basham, W.J.R., Marzadri, A., Tonina, D., Huber, C., 2019. A novel fiber optic system to map dissolved oxygen concentrations continuously within submerged sediments. Journal of Applied Water Engineering and Research 7 (3), 1e12. https://doi.org/10.1080/ 23249676.2019.1611495. Reeder, W.J., Quick, A.M., Farrell, T.B., Benner, S.G., Feris, K.P., Marzadri, A., Tonina, D., 2018a. Hyporheic source and sink of nitrous oxide. Water Resources Research 54 (7), 5001e5016. https://doi.org/10.1029/2018WR022564. Reeder, W.J., Quick, A.M., Farrell, T.B., Benner, S.G., Feris, K.P., Tonina, D., 2018b. Spatial and temporal dynamics of dissolved oxygen concentrations and bioactivity in the hyporheic zone. Water Resources Research 54 (3), 2112e2128. https://doi.org/10.1002/2017WR021388. Reisinger, A.J., Tank, J.L., Rosi-Marshall, E.J., Hall, R.O., Baker, M.A., 2015. The varying role of water column nutrient uptake along river continua in contrasting landscapes. Biogeochemistry 125 (1), 115e131. https://doi.org/ 10.1007/s10533-015-0118-z. Ren, J., Packman, A.I., 2004a. Modeling of simultaneous exchange of colloids and sorbing contaminants between streams and streambeds. Environmental Science and Technology 38 (10), 2901e2911. Ren, J., Packman, A.I., 2004b. Coupled stream-subsurface exchange of colloidal hematite and dissolved zinc, copper and phosphate. Environmental Science and Technology 39 (17), 6387e6394. Ren, J., Packman, A.I., 2007. Changes in fine sediment size distributions due to interactions with streambed sediments. Sedimentary Geology 202, 529e537. Ritzi, R.W., Dai, Z., Dominic, D.F., Rubin, Y.N., 2004. Spatial correlation of permeability in cross-stratified sediment with hierarchical architecture. Water Resources Research 40, W03513. Riva, M., Guadagnini, L., Guadagnini, A., Ptak, T., Martac, E., 2006. Probabilistic study of well capture zones distribution at the Lauswiesen field site. Journal of Contaminant Hydrology 88 (1), 92e118. Roche, K.R., Li, A., Bolster, D., Wagner, G.J., Packman, A.I., 2019. Effects of turbulent hyporheic mixing on reach-scale transport. Water Resources Research 55 (5), 3780e3795. https://doi.org/10.1029/2018WR023421.

I. Setting the scene: groundwater as ecosystems

References

85

Rousseau, G., Ancey, C., 2020. Scanning PIV of turbulent flows over and through rough porous beds using refractive index matching. Experiments in Fluids 61 (8), 1e24. https://doi.org/10.1007/s00348-020-02990-y. Rubol, S., Tonina, D., Vincent, L., Sohm, J.A., Basham, W., Budwig, R., Savalia, P., Kanso, E., Capone, D.G., Nealson, K.H., 2018. Seeing through porous media: an experimental study for unveiling interstitial flows. Hydrological Processes 32 (3), 402e407. https://doi.org/10.1002/hyp.11425. Runkel, R.L., 1998. One-dimensional Transport with Inflow and Storage (OTIS): A Solute Transport Model for Streams and Rivers. US Geological Survey, Water-Resources Investigations Report 98-4018, Denver, CO. Salarashayeri, A.F., Siosemarde, M., 2012. Prediction of soil hydraulic conductivity from particle-size distribution. International Journal of Geological and Environmental Engineering 61, 454e458. Salehin, M., Packman, A.I., Paradis, M., 2004. Hyporheic exchange with heterogeneous streambeds: laboratory experiments and modeling. Water Resources Research 40 (11), W11504. Sawyer, A.H., Cardenas, M.B., 2009. Hyporheic flow and residence time distributions in heterogeneous cross-bedded sediment. Water Resources Research 45, W08406. Sawyer, A.H., Cardenas, M.B., Buttles, J., 2011. Hyporheic exchange due to channel-spanning logs. Water Resources Research 47, W08502. Sheibley, R.W., Jackman, A.P., Duff, J.H., Triska, F.J., 2003. Numerical modeling of coupled nitrificatione denitrification in sediment perfusion cores from the hyporheic zone of the Shingobee River, MN. Advances in Water Resources 26, 977e987. Shen, H.V., Fehlman, H.M., Mendoza, C., 1990. Bed form resistance in open channel flows. Journal of Hydraulic Engineering 116 (6), 799e815. Shen, G., Yuan, J., Phanikumar, M.S., 2020. Direct numerical simulations of turbulence and hyporheic mixing near sediment-water interfaces. Journal of Fluid Mechanics 892 (A20). https://doi.org/10.1017/jfm.2020.173. Sherman, T., Roche, K.R., Richter, D.H., Packman, A.I., Bolster, D., 2019. A dual domain stochastic Lagrangian model for predicting transport in open channels with hyporheic exchange. Advances in Water Resources 125, 57e67. https://doi.org/10.1016/j.advwatres.2019.01.007. Singh, T., Gomez-Velez, J.D., Wu, L., Wörman, A., Hannah, D.M., Krause, S., 2020. Effects of successive peak flow events on hyporheic exchange and residence times. Water Resources Research 56 (8), e2020WR027113. https:// doi.org/10.1029/2020WR027113. Stanford, J.A., 2006. Landscapes and riverscapes. In: Hauer, F.R., Lamberti, G.A. (Eds.), Methods in Stream Ecology. Academic Press, San Diego, CA, pp. 3e21. Stanford, J.A., Ward, J.V., 1993. An ecosystem perspective of alluvial rivers: connectivity and the hyporheic corridor. Journal of the North American Benthological Society 12 (1), 48e60. Stanford, J.A., Lorang, M.S., Hauer, F.R., 2005. The shifting habitat mosaic of river ecosystems. Verhandlungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 29 (1), 123e136. https://doi.org/10.1080/ 03680770.2005.11901979. Stewart, R.J., Wollheim, W.M., Gooseff, M.N., Briggs, M.A., Jacobs, J.M., Peterson, B.J., Hopkinson, C.S., 2011. Separation of river networkescale nitrogen removal among the main channel and two transient storage compartments. Water Resources Research 47, W00J10. Stonedahl, S.H., Harvey, J.W., Packman, A.I., 2013. Interaction between hyporheic flow produced by stream meanders, bars and dunes. Water Resources Research 49, 5450e5461. Stonedahl, S.H., Harvey, J.W., Wörman, A., Salehin, M., Packman, A.I., 2010. A multi-scale model for integrating hyporheic exchange from ripples to meanders. Water Resources Research 46, W12539. Storey, R.G., Howard, K.W.F., Williams, D.D., 2003. Factor controlling riffle-scale hyporheic exchange flows and their seasonal changes in gaining stream: a three-dimensional groundwater model. Water Resources Research 39 (2), 1034. https://doi.org/10.1029/2002WR001367. Stuart, T.A., 1954. Spawning sites of trout. Nature 173, 354. Thibodeaux, L.J., Boyle, J.D., 1987. Bedform-generated convective transport in bottom sediment. Nature 325 (22), 341e343. Tonina, D., 2012. Surface water and streambed sediment interaction: the hyporheic exchange. In: Gualtieri, C., Mihailovic, D.T. (Eds.), Fluid Mechanics of Environmental Interfaces. CRC Press, Taylor and Francis Group, London, pp. 255e294.

I. Setting the scene: groundwater as ecosystems

86

3. Physical and biogeochemical processes of hyporheic exchange in alluvial rivers

Tonina, D., Buffington, J.M., 2007. Hyporheic exchange in gravel bed rivers with pool-riffle morphology: laboratory experiments and three-dimensional modeling. Water Resources Research 43, W01421. https://doi.org/10.1029/ 2005WR004328. Tonina, D., Buffington, J.M., 2009. Hyporheic exchange in mountain rivers I: mechanics and environmental effects. Geography Compass 3 (3), 1063e1086. https://doi.org/10.1111/j.1749-8198.2009.00226.x. Tonina, D., Buffington, J.M., 2011. Effects of stream discharge, alluvial depth and bar amplitude on hyporheic flow in pool-riffle channels. Water Resources Research 47 (8), W08508. https://doi.org/10.1029/ 2010WR009140. Tonina, D., de Barros, F.P.J., Marzadri, A., Bellin, A., 2016. Does streambed heterogeneity matter for hyporheic residence time distribution in sand-bedded streams? Advances in Water Resources 96, 120e126. https://doi.org/ 10.1016/j.advwatres.2016.07.009. Tonina, D., Marzadri, A., Bellin, A., 2015. Benthic uptake rate due to hyporheic exchange: the effects of streambed morphology for constant and sinusoidally varying nutrient loads. Water (Switzerland) 7 (2), 398e419. https:// doi.org/10.3390/w7020398. Trauth, N., Schmidt, C., Maier, U., Vieweg, M., Fleckenstein, J.H., 2013. Coupled 3-D stream flow and hyporheic flow model under varying stream and ambient groundwater flow conditions in a pool-riffle system. Water Resources Research 49 (9), 5834e5850. https://doi.org/10.1002/wrcr.20442. Trauth, N., Schmidt, J.C., Vieweg, M., Maier, U., Fleckenstein, J.H., 2014. Hyporheic transport and biogeochemical reactions in pool-riffle systems under varying ambient groundwater flow conditions. Journal of Geophysical Research: Biogeosciences 119, 910e928. Triska, F.J., Duff, J.H., Avanzino, R.J., 1993. Patterns of hydrological exchange and nutrient transformation in the hyporheic zone of a gravel bottom stream: examining terrestrial-aquatic linkages. Freshwater Biology 29, 259e274. Triska, F.J., Kennedy, V.C., Avanzino, R.J., Zellweger, G.W., Bencala, K.E., 1989a. Retention and transport of nutrients in a third-order stream: channel processes. Ecology 70, 1894e1905. Triska, F.J., Kennedy, V.C., Avanzino, R.J., Zellweger, G.W., Bencala, K.E., 1989b. Retention and transport of nutrients in a third-order stream in Northwestern California: hyporheic processes. Ecology 70 (6), 1893e1905. Tubino, M., 1991. Growth of alternate bars in unsteady flow. Water Resources Research 27 (1), 37e52. van Kampen, R., Schneidewind, U., Anibas, C., Bertagnoli, A., Tonina, D., Vandersteen, G., Luce, C., Krause, S., van Berkel, M., 2022. LPMLEneA frequency domain method to estimate vertical streambed fluxes and sediment thermal properties in semi-infinite and bounded domains. Water Resources Research 58 (3), e2021WR030886. https:// doi.org/10.1029/2021WR030886. Vaux, W.G., 1968. Intragravel flow and interchange of water in a streambed. Fishery Bulletin 66 (3), 479e489. Vieweg, M., Trauth, N., Fleckenstein, J.H., Schmidt, C., 2013. Robust optode-based method for measuring in situ oxygen profiles in gravelly streambeds. Environmental Science & Technology 47 (17), 9858e9865. https://doi.org/ 10.1021/es401040w. Vittal, N., Ranga Raju, K.G., Garde, R.J., 1977. Resistance of two-dimensional triangular roughness. Journal of Hydraulic Research 15 (1), 19e36. Voermans, J.J., Ghisalberti, M., & Ivey, G.N., 2018. The hydrodynamic response of the sediment-water interface to coherent turbulent motions. Geophysical Research Letters 45(19), 10,520e10,527. https://doi.org/10.1029/ 2018GL079850 Ward, A.S., Gooseff, M.N., Johnson, P.A., 2011. How can subsurface modifications to hydraulic conductivity be designed as stream restoration structures? Analysis of Vaux’s conceptual models to enhance hyporheic exchange. Water Resources Research 47 (8), W09418. Ward, A.S., Gooseff, M.N., Singha, K., 2010. Imaging hyporheic zone solute transport using electrical resistivity. Hydrological Processes 24, 948e953. White, D.S., 1993. Perspective on defining and delineating hyporheic zones. Journal of the North American Benthological Society 12 (1), 61e69. Winter, C.L., Tartakovsky, D.M., 2002. Groundwater flow in heterogeneous composite aquifers. Water Resources Research 38 (8). Winter, T.C., Harvey, J.W., Franke, O.L., Alley, W.M., 1998. Ground Water and Surface Water: A Single Resource. U.S. Geological Survey, Circular 1139, Denver, CO.

I. Setting the scene: groundwater as ecosystems

References

87

Wolke, P., Teitelbaum, Y., Deng, C., Lewandowski, J., Arnon, S., 2019. Impact of bed form celerity on oxygen dynamics in the hyporheic zone. Water 12 (1), 62. https://doi.org/10.3390/w12010062. Wondzell, S.M., 2011. The role of the hyporheic zone across stream networks. Hydrological Processes 25 (22), 3525e3532. Wondzell, S.M., Gooseff, M.N., 2013. Geomorphic controls on hyporheic exchange across scales: watersheds to particles. In: Shroder (Ed.-in-chief), J.F., Wohl (vol. Ed.), E. (Eds.), Treatise on Geomorphology, 9. Fluvial Geomorphology. Academic Press, San Diego, CA, pp. 203e218. Fluvial Geomorphology. Wondzell, S.M., Swanson, F.J., 1996. Seasonal and storm dynamics of the hyporheic zone of a 4th order mountain stream. 1: hydrologic processes. Journal of the North American Benthological Society 15, 3e19. Wörman, A., Packman, A.I., Johansson, H., Jonsson, K., 2002. Effect of flow-induced exchange in hyporheic zones on longitudinal transport of solutes in streams and rivers. Water Resources Research 38 (1), 2e15. Wörman, A., Packman, A.I., Marklund, L., Harvey, J.W., 2006. Exact three-dimensional spectral solution to surfacegroundwater interaction with arbitrary surface topography. Geophysical Research Letters 33, L07402. Wu, L., Gomez-Velez, J.D., Krause, S., Singh, T., Wörman, A., Lewandowski, J., 2020. Impact of flow alteration and temperature variability on hyporheic exchange. Water Resources Research 56 (3), e2019WR026225. https:// doi.org/10.1029/2019wr026225. Wuhrmann, K., 1972. River purification. In: Mitchell, R. (Ed.), Water Pollution Microbiology. Wiley-Interscience, New York, NY, pp. 119e151. Xia, X., Yang, Z., Zhang, X., 2009. Effect of suspended-sediment concentration on nitrification in river water: importance of suspended sediment e water interface. Environmental Science and Technology 43 (10), 3681e3687. https://doi.org/10.1021/es8036675. Yalin, M.S., 1964. Geometrical properties of sand waves. Journal of the Hydraulics Division 90, 105e119. Yuan, Y, Chen, X., Cardenas, M.B., Liu, X., Chen, L., 2021. Hyporheic exchange driven by submerged rigid vegetation: a modeling study. Water Resources Research 57 (6), e2019WR026675. https://doi.org/10.1029/ 2019WR026675. Zaramella, M., Packman, A.I., Marion, A., 2003. Application of the transient storage model to analyze advective hyporheic exchange with deep and shallow sediment beds. Water Resources Research 39 (7), 1198. Zarnetske, J.P., Gooseff, M.N., Bowden Morgan, J., Greenwald, M.J., Brosten, T.R., Bradford, J.H., McNamara, J.P., 2008. Influence of morphology and permafrost dynamics on hyporheic exchange in arctic headwater streams under warming climate conditions. Geophysical Research Letters 35, L02501. Zarnetske, J.P., Haggerty, R., Wondzell, S.M., Baker, M.A., 2011. Dynamics of nitrate production and removal as a function of residence time in the hyporheic zone. Journal of Geophysical Research: Biogeosciences 116, G01025. Zarnetske, J.P., Haggerty, R., Wondzell, S.M., Bokil, V.A., González-Pinzón, R., 2012. Coupled transport and reaction kinetics control the nitrate source-sink function of hyporheic zones. Water Resources Research 48, W11508. Zhou, Y., Ritzi, R.W., Soltanian, M.R., Dominic, D.F., 2014. The influence of streambed heterogeneity on hyporheic flow in gravelly rivers. Ground Water 52 (2), 206e216. Ziebis, W., Forster, S., Huettel, M., Jørgensen, B.B., Jorgensen, B.B., 1996. Complex burrows of mud shrimp Callianassa truncata and their geochemical impact in the sea bed. Nature 382 (6592), 619e622.

I. Setting the scene: groundwater as ecosystems

This page intentionally left blank

C H A P T E R

4 Ecological and evolutionary jargon in subterranean biology  Fiser3 David C. Culver1, Tanja Pipan2 and Ziga 1

Department of Environmental Science, American University, Washington, DC, United States; 2 ZRC SAZU, Karst Research Institute, Postojna, Slovenia; 3University of Ljubljana, Biotechnical Faculty, Department of Biology, Ljubljana, Slovenia

Introduction Just as lack of eyes and pigment and the increase in extra-optic sensory structures are the hallmarks of subterranean organisms, the terminology associated with subterranean life (troglobiont, stygobiont, etc.) is the hallmark of papers about subterranean life. With the exception of the topic of how subterranean species came to lose their eyes, discussions about the ecological classification of cave organisms in particular and subterranean organisms in general are probably as frequent as any other topic about subterranean life (e.g., Racovitza, 1907; Barr, 1968; Sket, 2008; Giachino and Vailati, 2017; Trajano and de Carvalho, 2017; Culver and Pipan, 2019a). Next in frequency, and perhaps surpassing discussions of ecological classification, is the question of how organisms came to be in subterranean habitats and how they managed to evolve at all (e.g., Racovitza, 1907; Howarth, 1980; Coineau and Boutin, 1992; Desutter-Grandcolas and Grandcolas, 1996; Culver and Pipan, 2019b). Almost simultaneously with the discovery of eyeless and pigmentless cave animals, ecological classification of cave dwellers began. In 1849, the Danish biologist Jørgen Schiødte proposed the first such classificatory scheme, based on the amount of light and the nature of the walls in the preferred habitat. The question arises why Schiødte and many who followed him found it necessary to have a classificatory scheme. If all cave (and by extension all subterranean) animals were without eyes and pigment, then presumably only one word would be necessary for all these species, e.g., cavernicole. However, the nearly universal presence of at least partially eyed and/or pigmented species in subterranean habitats (Pipan and Culver, 2012; Culver and Pipan, 2015) makes such a simple solution unrealistic and impractical. Classification schemes like Schiødte’s and others we take up below, do have the advantage of providing a common vocabulary for the field of speleobiological researchers, who come

Groundwater Ecology and Evolution, Second Edition https://doi.org/10.1016/B978-0-12-819119-4.00017-2

89

© 2023 Elsevier Inc. All rights reserved.

90

4. Ecological and evolutionary jargon in subterranean biology

from a wide variety of language groups and for whom English is typically not their first language. Disadvantages include an elaborate system that is nearly impenetrable to most readers and nonspecialists, imprecise and/or conflicting definitions, and equivalence of many terms to standard ecological and evolutionary terminology, a terminology many more readers are familiar with. Even though the speleobiological jargon can be fit into modern evolutionary thinking, its origins are often non-Darwinian and even anti-Darwinian (antiselectionist) (Romero, 2009). This leads to the perception that subterranean life is somehow subject to rules distinct from standard evolutionary and ecological processes. The terminology we examine is that of the extent of dependence on the subterranean environment (e.g., troglobionts), the mode of colonization and speciation (e.g., the Adaptive Shift Hypothesis), and the extent of modification for subterranean life (e.g., troglomorphy). Epistemologically, these are all hypotheses about the evolution of subterranean life. While we argue that there are far too many specialized terms for the evolution of subterranean life, it is probably true that there are not enough terms to describe subterranean habitats, given their unfamiliarity. The description of aquatic subterranean habitats themselves is covered in the chapter by Robertson et al. (this volume). Our goals are to (1) place the speleobiological terminology in a modern neo-Darwinian context, (2) suggest the minimal and judicious use of jargon, and (3) provide a glossary of ecological and evolutionary terms used in the study of subterranean aquatic systems.

Ecological classifications Schiødte’s classification and two possible explanations Schiødte (1849) proposed four categories: (1) shadow animals, (2) twilight animals, (3) obscure (¼aphotic) area animals, and (4) obscure area with flowstone animals. This categorization is based on the frequently described zonation of caves ranging from the entrance zone (shadow animals), to the twilight zone, to the zone of constant darkness (obscure area). Although he did not describe it as such, his categorization is a hypothesis where the distribution of organisms is in equilibrium with the environment. In spite of this very fundamental division of the cave habitat (see Howarth and Moldovan, 2018), there is little real evidence that cave dwellers show a zonation from eyed entrance animals to eyeless deep cave animals. Descriptions of zonation in caves are limited to terrestrial examples and are often nonquantitative (see Mohr and Poulson, 1966). In those few cases where quantitative data are available, eyed and pigmented individuals occur throughout the cave and eyeless and depigmented animals occur throughout most of the cave (Howarth and Stone, 1990; Tobin et al., 2013). The study of Tobin et al. (2013) provides a quantitative estimate of the importance of zonation in the distribution of species throughout the yeardthey found it accounted for 55% of the variation in species abundance. Kozel et al. (2019) provide a counterexample din Zguba jama in Slovenia, many eyeless, depigmented species were more common in shallower area of the cave. In other cases, zonation was completely lacking, notably in a large cave in Quintana Roo, Mexico, one with a minimal dark zone (Mejía-Ortíz et al., 2018). Equivalent patterns exist in the hyporheic zone. Gibert et al. (1990) showed the vertical zonation, with overlap of different species groups in the hyporheic zone of the Rhône River (Fig. 4.1A). Ward and Voelz (1997) provide data on the occurrence of different species in the

I. Setting the scene: groundwater as ecosystems

FIGURE 4.1 (a) Distribution of invertebrates in relation to the hyporheic zone: the case of the Rhône River, France. The dashed line indicates the extent of the hyporheic zone. (b) Examples of distribution of representative taxa in the phreatic, hyporheic, and benthic zones of the South Platte River in Colorado, USA. Species include strictly subterranean species such as the polychaete Troglochaetus beranecki, surface species such as the amphipod Crangonyx gracilis, as well as species with broader and intermediate distributions, such as the copepod Diacyclops crassicaudis. (a) From Gibert et al. (1990). Used with permission of Taylor & Francis. (b) Data from Ward and Voelz (1997).

I. Setting the scene: groundwater as ecosystems

92

4. Ecological and evolutionary jargon in subterranean biology

phreatic, hypogean, and benthic zones (Fig. 4.1B), the approximate equivalent of the entrance, twilight, and aphotic zones of caves. Some species were limited to a single zone and others were common in all three. Peralta-Maraver et al. (2018) were able to identify distinct benthic and hyporheic communities in a German stream but species from both communities cooccurred throughout the water column. A similar zonation pattern at a larger scale might exist when subterranean habitats with different degrees of isolation from the surface and different degrees of oligotrophy are compared, rather than different parts of the same cave. However, Culver and Pipan (2015) showed that the frequency of eyeless and depigmented species was no greater in relatively isolated and deep caves compared to the fauna of epikarst and seepage springs (Table 4.1). An entirely different hypothesis has been put forward to explain the presence of eyed, reduced eyed, and eyeless species in the same subterranean habitat, one that emphasizes not the equilibrium of distributions, but rather differences in age of the subterranean fauna. Different morphologies are present, according to this hypothesis, because of different lengths of time different species have been isolated in caves. The idea that degree of morphological modification and the age of colonization are correlated was popularized by Poulson (1963) for the amblyopsid fish in North American caves and Wilkens and Strecker (2017) for the Mexican cavefish, Astyanax mexicanus. However, the idea dates back at least to neoLamarckians such as Eigenmann (1909) and Jeannel (1950). Regardless of its origin, there is little contemporary support for the hypothesis. The molecular phylogeny of amblyopsid fish (Niemiller et al., 2012) does not correlate well with their morphological modification.

Modern ecological classifications While Schiødte’s classification scheme was the first one, modern classifications are based on the system developed by Schiner (1854) and Racovitza (1907). They recognized three categories: • Troglobites (troglobionts)dspecies whose habitat is exclusively in the subterranean domain and who show a preference for deeper parts of the habitat. • Troglophilesdspecies permanently inhabiting the subterranean domain, but preferably in superficial regions; they frequently reproduce there but may also be found outside. • Trogloxenesdoccasional or accidental visitors to caves attracted by humidity or food, but that do not live continuously or reproduce in caves. TABLE 4.1

Percent of eyeless aquatic species in different subterranean habitats. Epikarst

Hypotelminorheic

Caves

Number of sites

9

3

4

Geographic location

Slovenia (8), USA (1)

Croatia (1), Slovenia (1), USA (1)

UK (1), Bosnia & Hercegovina (1), USA (2)

Mean percent of eyeless aquatic 86 species

57

47

Range (minimum e maximum) 40e100

47e75

0e97

Data from Culver and Pipan (2015).

I. Setting the scene: groundwater as ecosystems

Ecological classifications

93

Racovitza’s definition of troglophiles included many types of speciesdthose that completed their life cycle in subterranean habitats but could also reproduce outside, and those species that required both surface and subterranean habitats to complete their life cycle. There is, however, ambiguity in his definitions of both troglophile and trogloxene. The trogloxene category is generally interpreted as species that are occasional visitors to caves. Trajano and de Carvalho (2017) define trogloxenes as species that have source populations in surface habitats and sink populations in caves. Pavan (1944), later endorsed by Sket (2008), suggested two kinds of troglophilesdeutroglophiles, which spend their entire life cycle in subterranean habitats or in surface habitats, depending on the population, and subtroglophiles, which either leave subterranean habitats periodically (e.g., bats foraging at night) or spend part of their life cycle in subterranean habitats and part in surface habitats [e.g., the stonefly Isocapnia (Stanford and Gaufin, 1974) and the grotto salamander Eurycea spelaea (Goricki et al., 2019)]. A widely used modification is that of Barr (1968), who basically renamed Pavan’s subtroglophiles as trogloxenes and eutroglophiles as troglophiles. Gibert et al. (1994) in the first edition of the enormously influential Groundwater Ecology book, proposed a scheme (Fig. 4.2) more like Racovitza’s scheme, with stygoxenes being accidental species, species permanently inhabiting the hyporheic (Pavan’s troglobites), species using both subterranean and surface habitats to complete their life cycle (amphibitesdPavan’s subtroglophiles), and stygophilic species that may either spend their entire life in either surface habitats or the hyporheic zone (Pavan’s eutroglophiles). This last category illustrates one of the problems with all of these schemesdthere are always cases that fit uncomfortably into any scheme. There does not seem to be an aquatic equivalent of species like many bats and crickets that leave caves most nights to forage. This may be because no one has looked for aquatic subterranean species in surface habitats at night, such as the benthos of streams or spring runs. Bressi et al. (1999) did report that the olm Proteus anguinus is frequently found at night in spring runs associated with caves. Gibert et al. (1994) were the first to use the terms stygobite (biont), stygophile, and stygoxene for aquatic subterranean species and restricting troglo- to terrestrial species. However, this has not been universally accepted (Sket, 2008). Finally, Gibert et al. (1994) distinguished two types of stygobiontsdubiquitous stygobionts and phreatobites (bionts). Phreatobites are species only found deep in alluvial aquifers, and not in other habitats such as caves or seepage springs. The temptation to give names for specialists living in other habitats, e.g., hypotelminorheobionts for hypotelminorheic specialist species, should be firmly resisted. A more recent elaboration and clarification of the ecological classification of subterranean species is that of Trajano (Trajano, 2012; Trajano and de Carvalho, 2017). She emphasized the importance of thinking about source and sink populations. Source populations are ones whose birth rate exceeds death rate while the opposite is true for sink populations, which are maintained by immigration from source populations (Pulliam, 1988). This is a very useful distinction in cases where a few individuals are observed in the “wrong” habitat, for example, a stygobiont found in a surface stream. As part of the definition of stygophiles (and troglophiles), Trajano and de Carvalho (2017) include the observation that source populations occur in both surface and subterranean habitats. As part of the definition of stygoxenes (and trogloxenes), they posit that they are “source populations in epigean habitats, with individuals using subterranean resources” but the opposite statement could also be maded that they are source populations in subterranean habitats using surface resources. For

I. Setting the scene: groundwater as ecosystems

94

4. Ecological and evolutionary jargon in subterranean biology

FIGURE 4.2 A classification of groundwater fauna based on its life cycle and its presence in surface and subterranean habitats. From Gibert et al. (1994).

I. Setting the scene: groundwater as ecosystems

Colonization and speciation

95

example, Isocapnia stoneflies spend nearly their entire life cycle in the hyporheic zone (Stanford and Gaufin, 1974). Other difficulties may arise in subterranean habitats such as the hypotelminorheic zone that are patchy and connected by dispersing individuals, i.e., a metapopulation in the sense of Levins (1969). In this model, which is very widely used for species with multiple, small, semiisolated populations, individual populations often go extinct and are recolonized from other sub-populations. The metapopulation consists of both source and sink populations, even though all of them are of the same type, e.g., hypotelminorheic. Finally, it may be difficult to objectively determine whether a population is a source or a sink, since it depends on the population growth rate, not population size (Pulliam, 1988).

Critique and alternative classifications Some of the difficulties with the above classifications become obvious when we hypothetically apply it to a surface habitat, for example lakes. Then we have for example, • lentobionts, species found only in lakes and specialized for life in lakes, • lentophiles, species found in lakes and elsewhere, with some modification for life in lakes, and • lentoxenes, species visiting lakes without modification for life in lakes. There is another way to categorize aquatic (and terrestrial) subterranean populations, and that is by the standard ecological terms of specialist and generalist. Specialist species in aquatic subterranean habitats include stygobionts and those stygoxenes that have an obligate dependence on subterranean habitats even though they also have an obligate dependence on surface habitats. Stygobionts can be even more specialized, with an obligate dependence on a particular aquatic subterranean habitat rather than subterranean habitats in general. Perhaps most stygobionts fall into this category, including what Gibert et al. (1994) termed phreatobites. Obvious examples of trogloxenic specialists are those bats that always hibernate in caves, such as Myotis grisescens. But there are aquatic examples as well. The grotto salamander Eurycea spelaea is always found in caves as adults but most larvae develop in surface stream and springs (Goricki et al., 2019). Interestingly, it is almost always listed as a stygobiont, when it is clearly a stygoxene, but just clearly a specialist. There are many generalist species of salamanders, ones that can complete their life cycles either in surface streams or cave streams. Examples include a number of species of Eurycea in North America, including E. lucifuga and E. longicauda (Goricki et al., 2019). While the generalist-specialist dichotomy does not capture the complexities of the association of species with subterranean habitats, it does have the advantage of using a common ecological terminology.

Colonization and speciation Climatic Relict and Adaptive Shift hypotheses and their historical background Several hypotheses were proposed for the origin of aquatic subterranean animals (reviewed by Coineau and Boutin, 1992; Holsinger, 2000; Stoch, 2004). Among these, the

I. Setting the scene: groundwater as ecosystems

96

4. Ecological and evolutionary jargon in subterranean biology

Climatic Relict Hypothesis (CRH) and Adaptive Shift Hypothesis (ASH) grew the deepest roots in the speleobiological community and stimulated the liveliest debates. The terms CRH and ASH imply that there is something inherently unique and special to the origin of subterranean life that escapes the general ecological and evolutionary vocabulary. The CRH postulates that subterranean species originated through the following scenario. A surface species exapted (sensu Gould and Vrba, 1982) to subterranean life experienced climate change, causing unfavorable environmental conditions in the species’ native (surface) habitat. Consequently, the species retreated underground, where conditions were more suitable, and formed subterranean populations. As its movement to the new habitat was forced, the colonization is said to be passive. The ancestral surface populations either died out or migrated to other surface habitats with more favorable conditions. In either case, surface and subterranean populations were geographically isolated and eventually allopatric speciation occurred. This hypothesis was inspired by the fact that many subterranean animals in temperate latitudes are geographic and/or phyletic relicts. It can be traced back to the early ideas of Jeannel (1950) and their summary in Vandel’s (1964) influential book on subterranean life. Originally, it was permeated with the idea that subterranean species are living fossils, primitive taxa, and evolutionary dead-ends. Such Lamarckism was shaken off after the hypothesis was modified and advanced by American speleobiologists in a neo-Darwinian fashion, starting with Barr (1960). He applied it to explain the distributional patterns of the Pseudoanophthalmus trechinae beetles in eastern North America. Pleistocene glacial fluctuations were since considered the dominant environmental change driving animals underground, especially terrestrial but also aquatic species (Juberthie, 1984; Barr and Holsinger, 1985). Later, the hypothesis embraced new discoveries of tropical relicts and associated non-Pleistocene climatic perturbations, such as late Tertiary droughts (e.g., Humphreys, 1993). So, in roughly 6 decades the CRH manifested in minor variants but its essentials remained constant, i.e., passive colonization and allopatric speciation. CRH was challenged with the development of the Adaptive Shift Hypothesis (ASH). This postulates that after a subterranean environment becomes available, either by its formation or expansion of an exapted surface species distribution, the latter colonizes the new habitat and exploits novel resources. It is not forced underground by unfavorable conditions at the surface and thus colonization is said to be active. A dramatic difference in environmental conditions of both habitats subsequently drives the adaptive divergence between surface and subterranean populations and leads to speciation despite geographic contact and gene flow. The essential components of ASH are thus active colonization and parapatric speciation. ASH was inspired by the discovery of young, nonrelictual subterranean faunas in the tropics, characterized by extant closely related diverging species pairs with parapatric distributions. It was championed by Howarth (1973, 1987) and Chapman (1982) based on their work on subterranean arthropods of Hawaii and Southeast Asia, respectively, among which Hawaiian planthoppers Oliarus stood out as the most prominent example. In years that followed, similar examples from Galapagos and Canary Islands (Oromí et al., 1991; Peck and Finston, 1993) but also of animals from temperate latitudes, such as Astyanax mexicanus (Wilkens and Hüppop, 1986) and Gammarus minus (Culver et al., 1995), provided further support to the ASH. Part of its pervasiveness in the community must have arisen due to the coincident

I. Setting the scene: groundwater as ecosystems

Colonization and speciation

97

shift in the general evolutionary doctrine from the view that speciation is invariably allopatric (Mayr, 1970) to the recognition of its nonallopatric modes (White, 1978). In summary, both CRH and ASH are hypotheses of evolutionary transition from surface to subterranean life. They were first proposed for terrestrial animals, later extended to aquatic ones, and the initial motivation seems to have been to explain biogeographical patterns. Differently from ecological classifications and troglomorphy, they did not start as strict verbal definitions by their original authors, but as ideas that were gradually developed as loosely formulated hypotheses. CRH and ASH agree that success of colonization depends on the exaptation of colonizing surface species, but assume different colonization and speciation modes. In the context of CRH and ASH the distinction of passive and active colonization has always been one of unfavorable versus nonunfavorable environmental conditions as drivers of colonization, and not one of involuntary displacement versus self-propelled locomotion. This later contrast predates the CRH and ASH, and was fueled by the once popular perspective that subterranean environment is inhospitable, harsh, and offers no benefits to the colonizers (Romero and Green, 2005). Last but not least, lumping of colonization and speciation, two distinct and largely independent processes, into one hypothesis is the source of many of the issues discussed next.

Critique of CRH and ASH Several difficulties accompany CRH and ASH, which might discourage nonspeleobiologists from considering the related literature. First is the confusion regarding what CRH and ASH are hypotheses about. Many authors are either vague or imprecise in their assertions. The phenomena they ascribe to both hypotheses are either too broad, such as evolution or origin of subterranean life, or too narrow, such as solely colonization or speciation. CRH and ASH are actually hypotheses of evolutionary transition from surface to subterranean life, more precisely, a particular combination of colonization and speciation mode. The origin of a subterranean species from a surface ancestor is however not an evolutionary dead-end. CRH and ASH thus ignore much of the complexity of the origin of subterranean life, i.e., the diversification and speciation of subterranean lineages within the subterranean realm (e.g., Leijs et al., 2012; Trontelj et al., 2012), or even the phenomenon of recolonization of surface habitats by subterranean species (e.g., Copilas-Ciocianu et al., 2018). Second, the CRH and ASH dichotomy implies that these are the sole competing alternatives of the transition from surface to subterranean life. However, several authors realized these hypotheses are neither competing nor sole alternatives. The relictual fauna of temperate regions and nonrelictual tropical fauna that inspired CRH and ASH, respectively, likely reflect two different time points of the same continuum where historical events (e.g., climatic and geological perturbations) obscured earlier patterns of an older fauna (Holsinger, 2000). Desutter-Grancolas and Grandcolas (1996) demonstrated that CRH and ASH are each defined by a unique combination of past environmental conditions (proxy for colonization mode), speciation mode, and present distribution, and that several other scenarios, such as active colonization followed by allopatric speciation, are reasonable alternatives as well. Third, the debate about passive versus active colonization mode has largely disappeared from the literature and is considered resolved or perhaps uninteresting. This owes to the realization that stochastic events of accidental displacement or the onset of diverse conditions at

I. Setting the scene: groundwater as ecosystems

98

4. Ecological and evolutionary jargon in subterranean biology

surface cannot explain the observation that surface-dwelling animals can and do enter underground all the time. Recognition of shallow subterranean habitats revealed that the subterranean environment is continuous with the surface and that the two are much better interconnected than previously thought (Culver and Pipan, 2014). Furthermore, movement of surface-dwelling species to subterranean habitats is now well-documented and apparently a ubiquitous phenomenon, continuously feeding the subterranean realm with a steady influx of colonists (Culver and Pipan, 2019b). Contemporary evidence thus translates the dilemmas of surface-subterranean colonization to general questions of invasion biology (Trontelj, 2018), with “why surface ancestors colonize subterranean habitats” giving way to “why certain colonizations are successful and others are not” (Ribera et al., 2018). Resolving the debate on colonization modes effectively reduces the distinction of CRH and ASH to allopatric versus parapatric speciation, in other words, whether divergence proceeds without or with gene flow (Niemiller et al., 2008). The necessity for related speleobiological jargon disappears at this point. Finally and most importantly, CRH and ASH do not give mutually exclusive predictions, making them inherently difficult if not impossible to falsify (Desutter-Grancolas, 1997a; Plath and Tobler, 2010; Niemiller and Soares, 2015). This remains true even when colonization is dissected out of both hypotheses and the CRH versus ASH discourse translates to the general question of the geography of speciation. Testing whether past speciation was allopatric or not is extremely difficult with currently available methods (Losos and Glor, 2003). For example, it is improbable to falsify nonallopatric speciation if surface ancestors are extinct or species geographic distributions changed significantly, which is the case in practically all older subterranean species. In such scenario, even when time calibrated lineage splits agree with independently calibrated periods of past climate change, like Leys et al. (2003) demonstrated for diving beetles from Australian calcretes, one still cannot exclude that speciation was parapatric and geographic isolation occurred after the fact. Similarly, allopatric speciation is hard to falsify in young adjacent surface-subterranean species pairs. Their current parapatry could be due to initial allopatry followed by range expansion and secondary contact and available methods cannot differentiate between the two scenarios (Coyne and Orr, 2004). However, promising approaches stemming from early evidence that present-day biodiversity and genomic patterns carry detectable and distinguishable fingerprints of specific speciation histories are emerging (e.g., Feder et al., 2013; Skeels and Cardellio, 2019). Until these are rigorous, CRH and ASH will remain unfalsifiable and with little power to explain how subterranean species originate from surface ancestors.

Alternative terminology: swinging the pendulum from geography to processes generating reproductive isolation As demonstrated above, clinging to CRH and ASH will give only limited insight into the origin of subterranean species. We believe time is ripe to reconcile both hypotheses with modern treatments of speciation. In the last 2 decades speciation research and classification underwent a major shift from the traditional process-free geographic modes to evolutionary processes driving divergence and generation of reproductive isolation, such as selection and genetic drift (Schluter, 2001; Via, 2001). Irrespective of why animals colonize underground and the geographic mode of subsequent speciation, subterranean habitats are

I. Setting the scene: groundwater as ecosystems

Morphological modification for subterranean life

99

lightless, stable, and usually food deprived. Transition from surface to subterranean life will thus always be characterized by a dramatic change in environment. It has been convincingly shown that in such cases reproductive isolation typically evolves as a result of divergent selection originating from ecological differences in environments (Nosil, 2012). According to modern classification this process is ecological speciation and can proceed in any geographic context. Speleobiologists have recognized that ASH includes ecological speciation (e.g., Trontelj, 2019), however it has been less clear that CRH does just as well, albeit in its allopatric mode. We propose ecological speciation is considered a null hypothesis of transition from surface to subterranean life. As any hypothesis it should be tested against its alternatives, in this case speciation without selection (Coyne and Orr, 2004; Schluter, 2009; Nosil, 2012; Langerhans and Riesch, 2013). Ecological speciation gives explicit predictions and tests for it are available (Nosil, 2012); the hypothesis thus meets the falsifiability criteria. Just as recognition of nonallopatric modes of speciation helped to establish ASH, which greatly extended our knowledge on the origin of subterranean animals, we believe it will be rewarding if the modern, process-oriented approach to speciation is more widely integrated into speleobiology. Shifting focus to testing the predictions of ecological speciation by posing questions like “do subterranean-derived traits emerge barriers to gene flow and constitute reproductive isolation and which traits are these?” will move us forward. So far, only few studies have tested reproductive barriers between a subterranean species and its surface ancestor (e.g., Tobler, 2009; Tobler et al., 2009; Riesch et al., 2011). As speciation occurs at the population e species interface, phylogenetically young systems, like Astyanax mexicanus, Poecillia mexicana, Asellus aquaticus, and Gammarus minus (see Chapters by Gross et al., Protas et al., and Fong et al., this volume), where transition from surface to subterranean environment is still ongoing or finished recently, will provide most insight into the process.

Should we retire the CRH and ASH as formal categories? Yes. This is not because the conundrum on the origin of subterranean species has been resolved, but because the terms raise several inherent issues, some of which are obsolete. Furthermore, we showed that what remains of CRH and ASH today has a suitable term in the general literature, i.e., ecological speciation, making speleobiology-specific terminology redundant. As CRH and ASH are historically important pillars of our field they will surely persist at least in discourses on its historical development. In other cases, we propose abandoning CRH and ASH as formal categories of classifications of origin of subterranean species. We expect this suggestion to be much less controversial than those proposed for other terms discussed in this chapter. In fact, CRH and ASH are already loosing viability as evident from a number of recent papers (e.g., Schilthuizen et al., 2005; Niemiller et al., 2008; Riesch et al., 2011; Borowsky and Cohen, 2013).

Morphological modification for subterranean life Troglomorphy and the nature of selection The ecological patterns of species occurrence in aquatic subterranean habitats are correlated, although not perfectly so, with morphological features. In particular, stygobionts

I. Setting the scene: groundwater as ecosystems

100

4. Ecological and evolutionary jargon in subterranean biology

(and troglobionts) typically have reduced or absent eyes and pigment, and stygophiles (and troglophiles) have eyes and pigment reduced to a lesser degree, if at all. There are other habitats where eyelessness is common, such as deep soil (Peck, 1990), so the connection is imperfect at best. Of course, there is a long-standing controversy about the causes of these reductions and losses. Among the suggested causes are use and disuse (Jeannel, 1950), neutral mutation and genetic drift (Wilkens and Strecker, 2017), natural selectiondacting either directly for energetic savings (Moran et al., 2014, 2015) or indirectly via pleiotropy (Jeffery, 2005), and phenotypic plasticity (Blin et al., 2018; Bilandzija et al., 2020). All of these hypothesized causes have a sense of inevitability of the direction of change, given enough time, which is in agreement with observations. Christiansen (1962) suggested that a separate terminology was needed to describe morphological patterns of subterranean species, and coined the now frequently used term “troglomorphy” to describe the suite of changes, both losses such as eyes, and gains, such as increases in extra-optic sensory structures (Table 4.2). It has come to include not only morphological traits, but also behavioral and physiological traits. Christiansen’s purpose was largely to inject neo-Darwinian concepts in subterranean biology, and he wrote in French, both because French biologists dominated subterranean biology, and because neoDarwinian concepts were not widely held in France at the time. Christiansen proposed three new terms to classify subterranean species morphologically: • Epigeomorphs, species showing no modification for subterranean life; • Ambimorphs, species showing some modification for subterranean life, but still retaining some morphological features of surface-dwelling species; and • Troglomorphs, species clearly modified for cave life, totally different from their surfacedwelling counterparts.

TABLE 4.2

Troglomorphic characters divided into ones that are elaborated and ones that are reduced in subterranean habitats.

Elaborated

Reduced

Specialization of sensory organs (e.g., touch, chemoreception)

Reduction of eyes, pigment, wings

Pseudophysogastry (Coleoptera)

Scale reduction or loss (teleost fishes)

Compressed or depressed body form (Hexapoda)

Loss of pigment cells and deposits

Increased egg volume

Cuticle thinning

Increased size (Collembola, Arachnida)

Reduction or loss of swim bladder (teleost fishes)

Unguis elongation (Collembola) Foot modification (Collembola, planthoppers) Elongate body form (teleost fishes, Arachnida) Depressed, shovel-like heads (teleost fishes, salamanders) Reduced femur length/cropy-empty live weight ratio (crickets) From Christiansen (2012).

I. Setting the scene: groundwater as ecosystems

Morphological modification for subterranean life

101

Fortunately, only the last term is widely accepted, because one could read the definitions in such a way that all but the most highly modified species in each lineage was an ambimorph. The advantages of the term troglomorph are: • It is a testable hypothesis about evolution in subterranean habitats. It is however not necessarily a hypothesis about natural selection for reduced characters because other forces, especially neutral mutation, can account these changes, at least for the reduction of eyes and pigment. • It effectively decouples morphology and habitat, and ensures that morphology is not used in ecological classifications. Troglomorphy refers to the suite of characters that change with isolation in subterranean habitats as a result of convergent forces of natural selection (Table 4.2), and is akin to the general evolutionary concept of convergence, which is typically used in the context of overall morphology, or facies. Some authors have questioned the decoupling of morphology (troglomorphy) and habitat specialization (e.g., troglobiont) and suggested troglomorphy be included in the definition of troglobiont (Peck, 2002). In addition, Trajano and de Carvalho (2017) discuss conceptual problems, but its usage has become widespread. Although the list in Table 4.2 includes many elaborated features, only eye and pigment loss are often taken as indicating troglomorphy, without considering other characters. This is not in the spirit of Christiansen’s definition, since it involved natural selection, and eye and pigment loss does not necessarily involve natural selection (Wilkens and Strecker, 2017). At about the same time as he coined the phrase troglomorphy, Christiansen (1961) developed the terms cave-dependent and cave-independent for individual morphological characters. Cave-dependent characters were ones that showed convergence among subterranean species, even when the effects of shared ancestry have been removed (see Christman et al., 1997). The presence of cave-dependent characters can also be tested, as we discuss below.

Case studies of troglomorphy Desutter-Grandcolas (1997b), on the basis of a cladistic analysis of the cricket clade (Amphiacustae), was perhaps the first to question whether there really was convergence (troglomorphy) among subterranean species. Her conclusion was that there was no evidence for troglomorphy aside from eye and pigment loss, although it should be noted that she analyzed crickets specialized for cave life but foraging for food on the surface, i.e., cave specialists that are trogloxenes. In their study of spring and cave populations of the amphipod Gammarus minus, Christman et al. (1997) found a similar pattern. They used the technique of phylogenetic subtraction to determine (1) the expected relative antennal and eye size for cave and spring populations in two drainage basins using an mtDNA based phylogeny, and (2) the deviation of observed morphology from the predicted morphology. Their results are summarized in Table 4.3. Based on mtDNA phylogeny, eye size of the two cave populations is somewhat smaller than that of the spring populations. This includes the phylogenetic effect, as well as the effect of natural selection or neutral mutation. However, the residual effects, with phylogeny removed, were both large and negative for the cave populations, indicating that they are smaller than expected from phylogenetic analysis, and subject to convergent selection. There

I. Setting the scene: groundwater as ecosystems

102 TABLE 4.3

4. Ecological and evolutionary jargon in subterranean biology

Results of analysis of four populations of Gammarus minus, partitioning antennal and eye size into phylogenetic components and residuals. If convergence is important, it will be seen in the residuals. Phylogeny based on mtDNA sequences. See Christman et al. (1997) for details. Y is the relative expected size based on phylogeny and Ɛ is the residual. Patterns of the residuals may indicate homoplasy. Antenna

Eye

Y

Ɛ

Y

Ɛ

0.0125

0.1691

0.3601

0.462

Benedict cave

0.1122

0.6632

0.0751

1.344

Organ spring

0.0324

0.0132

0.4536

0.1945

0.0962

0.7159

0.0559

1.3385

Population Davis spring

Organ cave

was a different pattern with respect to antenna size. Amphipods from one spring (Davis Spring) and one cave (Organ Cave, in another basin) had phylogenetically small antennae. Unlike the case with eye size, residuals showed no evidence of convergence. Simcic and Sket (2019) found another case, this one involving a physiological trait, where subterranean species did not show convergence. They compared metabolic rates of a surfaceand subterranean-living Niphargus species pair and Asellus aquaticus population pair and found that metabolic rates were not reduced in either subterranean representative, contrary to expectation. The most extensive study to date of the prevalence of convergence (troglomorphy) is that of Konec et al. (2015) and Protas et al. (this volume). Konec et al. compared the morphology of two surface-subterranean population pairs of the isopod Asellus aquaticus from two drainages in Slovenia and Romania for a total of 63 morphological characters. Their results are summarized in Table 4.4. The most common pattern was one where only one population changed, which happened in 30 traits (48%); convergence occurred in 18 traits (29%), and divergence was found in two traits (3%). Protas et al. (this volume) extended the analysis with four additional population pairs (mostly from Slovenia), of which two included only a partially

TABLE 4.4

Summary of character changes in Slovenian and Romanian cave populations of Asellus aquaticus.

Type of change

Number of traits

Percentage of traits

Convergence

18

29

Divergence

2

3

Change in one population only (autapomorphy)

22 in Slovenia, 8 in Romania

48

Increase in variance, mean unchanged

2 in Romania

3

No change

11

17

Adapted from Konec et al. (2015).

I. Setting the scene: groundwater as ecosystems

Overall recommendations

103

depigmented cave population. Considering only the four pairs with a completely depigmented cave population, 39 traits showed a significant change from its surface counterpart in at least three pairs. A total of 13 traits showed divergence among cave populations, 15 were convergently reduced, and only 11 were convergently elaborated. The work of Fiser et al. (2012) and Trontelj et al. (2012) demonstrated that morphological variability among Niphargus amphipod species in both interstitial and cave communities was greater, not less, than expected by chance. Thus, divergence rather than convergence was occurring at this scale. They did show that species in different caves tended to share particular morphologies, e.g., lake giants, a form of convergence, but at a different scale.

Critique and alternative classifications Given the real data on convergence and troglomorphism, there is evidence that convergence does occur but that it by no means predominates. Convergence due to selection occurs because of a shared selective environment. Pipan and Culver (2012) argue that only the absence [or near absence (Mejìa-Ortìz et al., 2018)] of light is shared among all subterranean environments. Low food resources are often invoked as a nearly universal feature of caves and other subterranean environments (Kovác, 2018), but there are many cases of relatively high resource levels in subterranean habitats that also have species with reduced eyes and pigment (Culver and Pipan, 2014). On the other hand, there are factors that promote divergence, including interspecific competition, differing habitat dimensions, flux of organic matter, and proximity to the surface. Additionally, unique adaptations (autapomorphies), which predominated in Konec et al.’s study, may be common in subterranean communities in general (see Bichuette et al., 2015). The newly emerging paradigm of a mixture of convergence and divergence differs profoundly from the old troglomorphy paradigm, but it does share the feature that morphology of subterranean organisms is molded by natural selection, rather than genetic drift or other non-Darwinian forms of evolution. For example, in Konec et al.’s (2015) study, 52 of the 63 morphological characters measured showed evidence of directional selection in the subterranean populations, strong support for the neo-Darwinian school of evolution.

Overall recommendations If there were generally agreed upon definitions of speleobiological jargon, and these terms had no equivalent in the general ecological and evolutionary literature, then the use and continued refinement of these terms would be justified. However, neither of these conditions are met. There continue to be discussions and disputes about terminology (see especially Sket, 2008; Giachino and Vailati, 2017; Trajano and de Carvalho, 2017), and while these discussions are interesting, it is not clear that refinement of terminology actually increases understanding of the underlying ecological and evolutionary processes. Of course, these terms will never entirely disappear but a reduction in their use and an increase in the use of the standard neo-Darwinian vocabulary should speed up the integration of subterranean biology studies into the broader fields of ecology and evolutionary biology, as well as increase readership and citations of cave biology related papers (Martinez

I. Setting the scene: groundwater as ecosystems

104

4. Ecological and evolutionary jargon in subterranean biology

and Mammola, 2021). Historically, subterranean biology developed along a separate path due to the apparent importance of Lamarckian processes involved in the loss and reduction of structures. These non-Darwinian ideas persisted well into the mid-20th century at least in France (Jeannel, 1950; Vandel, 1964). The neo-Darwinian school of subterranean biology, developed by Barr, Christiansen, and Poulson in the 1960s in North America, signaled the beginning of the reintegration of subterranean biology into the mainstream (Mammola, 2019; Mammola et al., 2020). This process continues, as witnessed by the ever expanding number of papers on subterranean biology published in mainstream journals, thus enriching the wider community with knowledge gained from the unique subterranean fauna more effectively. Putting the scientific romanticism to a more practical perspective, such practice will lead to increased number of citations and open better funding options, a crucial element fueling new discoveries in every field.

Glossaries Aim and scope of two glossaries We provide definitions and commentary on specialized ecological and evolutionary terms used in aquatic subterranean biology. We have excluded a number of terms little if ever used. Both Sket (2008) and Trajano and de Carvalho (2017) discussed a number of these. We have also not included the very large number of terms used to describe aquatic subterranean habitats, which are covered by Robertson et al. (this volume). Many of the terms defined below are ones that we recommend be used rarely if ever, and we have included them as a guide to the literature in what we call the Retired Speleobiological Glossary. As a guide to a transition to a more general ecological and evolutionary terminology, we included the most relevant terms in what we call the Eco-Evo Glossary. We provide their common definitions, although we recognize that other definitions exist and should be consulted.

Eco-Evo Glossary Allopatric speciation Evolution of geographically isolated populations, with little or no possibility of mutual gene flow, into distinct species. Convergence The independent evolution of similar traits in distinct evolutionary lineages, often as a result of similar selective pressures. Troglomorphy is the occurrence of convergence, especially in morphology, due to natural selection acting upon subterranean populations or species. Divergence The independent evolution of different traits in distinct evolutionary lineages, often as a result of different selective pressures. Although widespread among subterranean species, it was not given a separate name in speleobiology. Ecological generalist Species that generally lives in a wide range of habitats and feeds on a wide range of food sources. Troglophiles (both eutroglophiles and subtroglophiles) fall into this category as well as trogloxenes that do not depend on subterranean habitats to complete their life cycle. Ecological specialist Species that generally occupies a very restricted range or even a single habitat and feeds on a small range or even a single food source. Troglobionts and those trogloxenes with an absolute dependence on subterranean habitats to complete their life cycle are in this category. Ecological speciation Evolution of reproductive isolation between populations due to ecologically based divergent selection between environments.

I. Setting the scene: groundwater as ecosystems

Retired Speleobiological Glossary

105

Exaptation A trait, feature, or structure of an organism or taxonomic group that takes on a function when none previously existed or that differs from its original function. Parapatric speciation Evolution of geographically separate but adjacent populations, with limited possibility of mutual gene flow, into distinct species. Speciation The process by which populations become distinct species by evolving mutual reproductive isolation. Sympatric speciation Evolution of populations occupying the same geographical area, with unlimited possibility of mutual gene flow, into distinct species.

Retired Speleobiological Glossary Accidental Individuals that enter subterranean habitats by chance and are unable to survive and reproduce there. They form sink populations, but sometimes apparently accidental species successfully establish reproducing populations, as is the case with the frog Rana iberica in the cave Serra da Estrela in Portugal (Rosa & Penado, 2013). It is the fourth term (together with trogloxene, troglophile, and troglobiont) in many classification schemes, such as Barr’s (1968). In the original Schiner-Racovitza scheme, they are equivalent to trogloxenes. Adaptive Shift Hypothesis A hypothesis originally championed by Howarth (1973) that surface species actively colonized subterranean habitats to exploit new resources, and that subsequent speciation was parapatric. Ambimorph A term coined by Christiansen (1962) for a species with a morphology intermediate between that of a surface dweller and a highly modified subterranean dweller (troglomorph). Its use is rare and would introduce a lot of confusion since only the most extreme case of modification in a lineage would be a troglomorph. For example, only Speoplatyrhinus poulsoni would be a troglomorph in the Amblyopsidae fish lineage. All others, such as Amblyopsis spelaea, would be ambimorphs. Amphibites (biont) Introduced by Gibert et al. (1994), these are species (aquatic insects) that complete part of their life cycle in either phreatic or hyporheic waters (both aphotic) and part of their life cycle in the benthos and other surface waters. The classic case is the stonefly Isocapnia (Stanford & Gaufin, 1974) from the Flathead River in Montana, USA. These species spend most of their life cycle in the deep hyporheic, dispersing to the benthic in order to emerge as mating adults. Sket (2008) recommends, on a linguistic basis, use of the suffix “-biont” rather than “-bite” for this and other terms. Cave-dependent character Introduced by Christiansen (1961), it denotes a character that is modified during the course of isolation in a subterranean habitat. He used it in the a priori sense of being predicted change, such as the elongation of relative appendage length. It can also be used in the a posteriori sense of discovering a cavedependent character after morphological analysis (Konec et al., 2015). Cavernicole Generally taken to mean populations reproducing in caves (or subterranean habitats in general), although some authors include nonreproducing accidentals in the definition (Humphreys, 2000). Its use in the former sense seems more appropriate. Climatic Relict Hypothesis A hypothesis popularized by Barr (1960), but drawing from ideas of R. Jeannel and A. Vandel, that surface species passively colonized subterranean habitats because of unfavorable surface conditions caused by changed climate which also resulted in extinction or migration of the surface population(s), and thus subsequent speciation was allopatric. Epigeomorph A rarely used term introduced by Christiansen (1962) for individuals and species without morphological modifications for subterranean life, in contrast with ambimorphs and troglomorphs. Eutroglophiles Initially used by Pavan (1944) and resurrected by Sket (2008), these are species that can complete their life cycles in subterranean habitats or in surface habitats. This is essentially the troglophile category of many other authors, such as Barr (1968). Phreatobite (biont) Species or populations only found in the phreatic zone and unable to complete their life cycle elsewhere, even in other subterranean habitats. Gibert et al. (1994) state that “phreatobites are stygobionts restricted to the deep groundwater substrate of alluvial aquifers.” The term is rarely used. Similar terms could be suggested for other aquatic subterranean habitats such as epikarst, but fortunately no one has done so yet. Culver and Pipan (2014) use the phrase epikarst specialists rather than introducing new terminology such as epikarstobite. Sket (2008) recommends, on a linguistic basis, use of the suffix “-biont” rather than “-bite” for this and other terms.

I. Setting the scene: groundwater as ecosystems

106

4. Ecological and evolutionary jargon in subterranean biology

Stygobite (biont) Species or populations that are unable to complete their life cycle outside of aquatic subterranean habitats. For the most part, all authors agree with this definition, although some (e.g., Sket, 2008) prefer the use of troglobite (troglobiont) for both aquatic and terrestrial species to avoid an unnecessary proliferation of terms. Sket (2008) recommends, on a linguistic basis, use of the suffix “-biont” rather than “-bite” for this and other terms. Stygomorph A term sometimes used for the suite of morphological characters that are convergent among subterranean aquatic species, although most authors seem to use the term troglomorph (see below). Both terms are hypotheses about the expected outcome of evolution in subterranean environments. Expected convergent morphologies include both reduced features, such as eyes and pigment, and elaborated features, such as elongation of appendages (see Table 4.2). Stygophile Facultative permanent species, resident of aquatic subterranean habitats. It can also occur in surface habitats. Eustygophile according to the Pavan-Sket scheme (Sket, 2008), but this term is almost not used. According to Trajano and de Carvalho (2017), both subterranean and surface populations are source populations. Stygoxene Species using both surface and aquatic subterranean habitats during their life cycle. The transition between the two habitats can occur once during the life cycle (e.g., emergence of Isocapnia from the hyporheic) or on a daily basis. The daily transition appears to be rare among aquatic species but is common among terrestrial species, including many bats. Trajano and de Carvalho (2017) suggest the surface populations are source populations, but more accurately, both source and sink populations occur in both habitats. According to the SchinerRacovitza scheme, stygoxenes (trogloxenes) are species that are accidentally and sporadically found in aquatic subterranean habitats. Subtroglophile In the Pavan-Sket scheme, species that use both surface and aquatic subterranean habitats during their life cycle. They are the equivalent of trogloxenes (stygoxenes) in other classifications. Troglobite (biont) Obligate permanent resident of terrestrial subterranean habitats. Used by some authors (e.g., Sket, 2008) for aquatic subterranean species (stygobionts) as well. Except for this distinction, the term is used in the same way by all authors. Sket (2008) recommends, on a linguistic basis, use of the suffix “-biont” rather than “-bite” for this and other terms. Troglodyte A human cave dweller, occasionally incorrectly applied to cave populations of other species. Troglomorph (troglobiomorph) A term for the suite of morphological characters that are convergent among subterranean species. It is a hypothesis about the expected outcome of evolution in subterranean environments. Expected convergent morphologies include both reduced features, such as eyes and pigment, and elaborated features, such as elongation of appendages (see Table 4.2). Troglophile Facultative permanent species, resident of terrestrial subterranean habitats, but it can be used for aquatic subterranean species as well. They can also occur in surface habitats. They are eutroglophile according to the Pavan-Sket scheme (Sket, 2008). According to Trajano and de Carvalho (2017), both subterranean and surface populations are source populations. Trogloxene Species using both surface and subterranean terrestrial habitats during their life cycle, and some authors (e.g., Sket, 2008) use the term for aquatic species as well. The transition between the two habitats can occur once during the life cycle or on a daily basis. The daily transition appears to be rare among aquatic species but is common among terrestrial species, including many bats. Trajano and de Carvalho (2017) suggest the surface populations are source populations, but more accurately, both source and sink populations occur in both habitats. According to the Schiner-Racovitza scheme, trogloxenes are species that are accidentally and sporadically found in terrestrial subterranean habitats.

Acknowledgments The work of T.P. was supported by the EU H2020 projects eLTER PPP and eLTER PLUS and RIeSIeLifeWatch. The  was supported by the Slovenian Research Agency through Research Core Funding P1-0184 and research work of Z.F. project N1-0069. We thank S. Mammola and F. Malard for constructive comments that improved this chapter.

References Barr, T.C., 1960. A synopsis of cave beetles of the genus Pseudanophthalmus of the Mitchell Plain in southern Indiana (Coleoptera, Carabidae). The American Midland Naturalist 63, 307e320.

I. Setting the scene: groundwater as ecosystems

References

107

Barr, T.C., 1968. Cave ecology and the evolution of troglobites. Evolutionary Biology 2, 35e102. Barr, T.C., Holsinger, J.R., 1985. Speciation in cave faunas. Annual Review of Ecology and Systematics 16, 313e337. Bichuette, M.E., Rantin, B., Hingst-Zaher, E., Trajano, E., 2015. Geometric morphometrics throws light on evolution of the subterranean catfish Rhamdiopsis krugi (Teleostei: Siluriformes: Heptapteridae) in eastern Brazil. Biological Journal of the Linnean Society 114, 136e151.  Biland zija, H., Hollifield, B., Steck, M., Meng, G., Ng, M., Koch, A.D., Gracan, R., Cetkovi c, H., Porter, M.L., Renner, K.J., Jeffery, W., 2020. Phenotypic plasticity as an important mechanism of cave colonization and adaptation in Astyanax cavefish. eLife 9, e51830. Blin, M., Tine, E., Meister, L., Elipot, Y., Bibliowicz, J., Espinasa, L., Rétaux, S., 2018. Developmental evolution and developmental plasticity of the olfactory epithelium and olfactory skills in Mexican cavefish. Developmental Biology 441 (2), 242e251. Borowsky, R., Cohen, D., 2013. Genomic consequences of ecological speciation in Astyanax cavefish. PLoS One 8 (11), e79903. Bressi, L., Aljancic, M.M., Lapini, L., 1999. Notes on the presence and feeding of Proteus anguinus Laurenti 1768, outside caves. Rivue Idrobiologia 38, 431e435. Chapman, P., 1982. The origin of troglobites. Proceedings of the University of Bristol Speleological Society 16, 133e141. Christiansen, K.A., 1961. Convergence and parallelism in cave Entomobryinae. Evolution 15, 288e301. Christiansen, K.A., 1962. Proposition pour la classification des animaux cavernicoles. Spelunca 2, 76e78. Christiansen, K.A., 2012. Morphological adaptations. In: White, W.B., Culver, D.C. (Eds.), Encyclopedia of Caves, second ed. Academic/Elsevier Press, Amsterdam, pp. 517e528. Christman, M.C., Jernigan, R.W., Culver, D.C., 1997. A comparison of two models for estimating phylogenetic effect on trait variation. Evolution 51, 262e266. Coineau, N., Boutin, C., 1992. Biological processes in space and time. Colonization, evolution and speciation in interstitial stygobionts. In: Camacho, A.I. (Ed.), The Natural History of Biospeleology. Monografías 7, Museo Nacional de Ciencias Naturales, Madrid, Spain, pp. 423e452. Copilas-Ciocianu, D., Fiser, C., Borza, P., Petrusek, A., 2018. Is subterranean lifestyle reversible? Independent and recent large-scale dispersal into surface waters by two species of the groundwater amphipod genus Niphargus. Molecular Phylogenetics and Evolution 119, 37e49. Coyne, J.A., Orr, H.A., 2004. Speciation. Sinauer Associates, Sunderland, MA. Culver, D.C., Kane, T.C., Fong, D.W., 1995. Adaptation and Natural Selection in Caves: The Evolution of Gammarus Minus. Harvard University Press, Cambridge. Culver, D.C., Pipan, T., 2014. Shallow Subterranean Habitats. Ecology, Evolution, and Conservation. Oxford University Press, Oxford. Culver, D.C., Pipan, T., 2015. Shifting paradigms of the evolution of cave life. Acta Carsologica 44, 415e425. Culver, D.C., Pipan, T., 2019a. Ecological and evolutionary classifications of subterranean organisms. In: White, W.B., Culver, D.C., Pipan, T. (Eds.), Encyclopedia of Caves, third ed. Academic/Elsevier Press, Amsterdam, pp. 376e379. Culver, D.C., Pipan, T., 2019b. The Biology of Caves and Other Subterranean Habitats, second ed. Oxford University Press, Oxford. Desutter-Grandcolas, L., 1997a. Studies in cave life evolution: a rationale for future theoretical developments using phylogenetic inference. Journal of Zoological Systematics and Evolutionary Research 35, 23e31. Desutter-Grandcolas, L., 1997b. Are troglobitic taxa troglobiomorphic? A test using phylogenetic inference. International Journal of Speleology 26, 1e19. Desutter-Grandcolas, L., Grandcolas, P., 1996. The evolution toward troglobitic life: a phylogenetic reappraisal of climatic relict and local habitat shift hypotheses. Mémoires de Biospéologie 23, 57e63. Eigenmann, C.H., 1909. Cave Vertebrates of America. A Study in Degenerative Evolution. Carnegie Institution of Washington, Washington, DC. Feder, J.L., Flaxman, S.M., Egan, S.P., Comeault, A.A., Nosil, P., 2013. Geographic mode of speciation and genomic divergence. Annual Review of Ecology, Evolution, and Systematics 44, 73e97. Fiser, C., Blejec, A., Trontelj, P., 2012. Niche-based mechanisms operating within extreme habitats: a case study of subterranean amphipod communities. Biology Letters 8, 578e581.

I. Setting the scene: groundwater as ecosystems

108

4. Ecological and evolutionary jargon in subterranean biology

Giachino, P.M., Vailati, D., 2017. Considerations on biological and terminological aspects of the subterranean and endogean environments. Diversity, correlations and faunistic interchange. Atti della Accademia Nazionale Italiana di Entomologia 65, 157e166. Gibert, J., Dole-Olivier, M.J., Marmonier, P., Vervier, P., 1990. Surface water/groundwater ecotones. In: Naiman, R.J., Décamps, H. (Eds.), Ecology and Management of Aquatic-Terrestrial Ecotones. Parthenon Publishing, Carnforth, UK, pp. 199e225. Gibert, J., Stanford, J.A., Dole-Olivier, M.J., Ward, J.V., 1994. Basic attributes of groundwater ecosystems and prospects for research. In: Gibert, J., Danielopol, D.L., Stanford, J.A. (Eds.), Groundwater Ecology. Academic Press, San Diego, pp. 8e40.  Niemiller, M.L., Fenolio, D.B., Gluesenkamp, A.G., 2019. Salamanders. In: White, W.B., Culver, D.C., Goricki, S., Pipan, T. (Eds.), Encyclopedia of Caves, third ed. Elsevier/Academic Press, Amsterdam, pp. 871e884. Gould, S.J., Vrba, E.S., 1982. Exaptationda missing term in the science of form. Paleobiology 8, 4e15. Holsinger, J.R., 2000. Ecological derivation, colonization, and speciation. In: Wilkens, H., Culver, D.C., Humphreys, W.F. (Eds.), Ecosystems of the World. Vol. 30. Subterranean Ecosystems. Elsevier, Amsterdam, pp. 399e415. Howarth, F.G., 1973. The cavernicolous fauna of Hawaiian lava tubes, 1. Introduction. Pacific Insects 15, 139e151. Howarth, F.G., 1980. The zoogeography of specialized cave animals: a bioclimatic model. Evolution 28, 365e389. Howarth, F.G., 1987. The evolution of non-relictual tropical troglobites. International Journal of Speleology 16, le16. Howarth, F.G., Moldovan, O.T., 2018. The ecological classification of cave animals. In: Moldovan, O.T., Kovác, L., Halse, S. (Eds.), Cave Ecology. Springer, Cham, Switzerland, pp. 41e67. Howarth, F.G., Stone, F.D., 1990. Elevated carbon dioxide levels in Bayliss Cave, Australia: implications for the evolution of obligate cave species. Pacific Science 44, 207e218. Humphreys, W.F., 1993. The significance of the subterranean fauna in biogeographical reconstruction: examples from Cape Range peninsula, Western Australia. In: Humphreys, W.F. (Ed.), The Biogeography of Cape Range, Western Australia. Records of the Western Australian Museum, Perth, pp. 165e192. Supplement 45. Humphreys, W.F., 2000. Background and glossary. In: Wilkens, H., Culver, D.C., Humphreys, W.F. (Eds.), Subterranean Ecosystems. Elsevier, Amsterdam, pp. 3e14. Jeannel, R., 1950. La marche de l’Évolution. Presses Universitaires de France, Paris. Jeffery, W.R., 2005. Evolution of eye degeneration in cavefish: the return of pleiotropy. Subterranean Biology 3, 1e11. Juberthie, C., 1984. La colonisation du milieu souterrain; théories et modèles, relations avec la spéciation et l’évolution souterraine. Mémoires de Biospéologie 11, 65e102. Konec, M., Prevorcnik, S., Sarbu, S.M., Verovnik, R., Trontelj, P., 2015. Parallels between two geographically and ecologically disparate cave invasions by the same species, Asellus aquaticus (Isopoda, Crustacea). Journal of Evolutionary Biology 28, 864e875. Kovác, L., 2018. Caves as oligotrophic ecosystems. In: Moldovan, O.T., Kovác, L., Halse, S. (Eds.), Cave Ecology. Springer, Cham, Switzerland, pp. 297e307. Kozel, P., Pipan, T., Mammola, S., Culver, D.C., Novak, T., 2019. Distributional dynamics of a specialized subterranean community oppose the classical understanding of the preferred subterranean habitats. Invertebrate Biology 138 (3), e12254. Langerhans, R.B., Riesch, R., 2013. Speciation by selection: a framework for understanding ecology’s role in speciation. Current Zoology 59, 31e52. Leijs, R., van Nes, E.H., Watts, C.H., Cooper, S.J.B., Humphreys, W.F., Hogendoorn, K., 2012. Evolution of blind beetles in isolated aquifers: a test of alternative modes of speciation. PLoS One 7 (3), e34260. Levins, R., 1969. Some demographic and genetic consequences of environmental heterogeneity for biological control. Bulletin of the Entomological Society of America 15 (3), 237e240. Leys, R., Watts, C.H.S., Cooper, S.J.B., Humphreys, W.F., 2003. Evolution of subterranean diving beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 57, 2819e2834. Losos, J.B., Glor, R.E., 2003. Phylogenetic comparative methods and the geography of speciation. Trends in Ecology & Evolution 18, 220e227. Mammola, S., 2019. Finding answers in the dark: caves as models in ecology fifty years after Poulson and White. Ecography 42, 1331e1351. Mammola, S., Amorim, I.R., Bichuette, M.E., Borges, P.A.V., Cheeptham, N., Cooper, S.J.B., Culver, D.C.,  Fong, D.W., Griebler, C., Jeffery, W.R., Jugovic, J., Deharveng, L., Eme, D., Ferreira, R.L., Fiser, C., Fiser, Z.,

I. Setting the scene: groundwater as ecosystems

References

109

Kowalko, J.E., Lilley, T.M., Malard, F., Manenti, R., Martínez, A., Meierhofer, M.B., Niemiller, M.L., Northup, D.E., Pellegrini, T.G., Pipan, T., Protas, M., Reboleira, A.S.P.S., Venarsky, M.P., Wynne, J.J., Zagmajster, M., Cardoso, P., 2020. Fundamental research questions in subterranean biology. Biological Reviews 95 (6), 1855e1872. Martinez, A., Mammola, S., 2021. Specialized terminology reduces the number of citations of scientific papers. Proceedings of the Royal Society B 288 (1948), 20202581. Mayr, E., 1970. Populations, Species, and Evolution. Harvard University Press, Cambridge. Mejía-Ortíz, L.M., Pipan, T., Culver, D.C., Sprouse, P., 2018. The blurred line between photic and aphotic environments: a large Mexican cave with almost no dark zone. International Journal of Speleology 37, 69e80. Mohr, C.E., Poulson, T.L., 1966. The Life of the Cave. McGraw-Hill, New York. Moran, D., Softley, R., Warrant, E.J., 2014. Eyeless Mexican cavefish save energy by eliminating the circadian rhythm in metabolism. PLoS One 9 (9), e107877. Moran, D., Softley, R., Warrant, E.J., 2015. The energetic cost of vision and the evolution of eyeless Mexican cavefish. Science Advances 1 (8), e1500363. Niemiller, M.L., Soares, D., 2015. Cave environments. In: Riesch, R., Tobler, M., Plath, M. (Eds.), Extremophile Fishes: Ecology, Evolution, and Physiology of Teleosts in Extreme Environments. Springer, Cham, Switzerland, pp. 161e191. Niemiller, M.L., Fitzpatrick, B.M., Miller, B.T., 2008. Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies. Molecular Ecology 17, 2258e2275. Niemiller, M.L., Fitzpatrick, B.M., Shah, P., Schmitz, L., Near, T.J., 2012. Evidence for repeated loss of selective constraint in rhodopsin of amblyopsid cavefishes (Teleostei: Amblyopsidae). Evolution 67, 732e748. Nosil, P., 2012. Ecological Speciation. Oxford University Press, Oxford. Oromí, P., Martin, J.L., Medina, A.L., Izquierdo, I., 1991. The evolution of the hypogean fauna in the Canary Islands. In: Dudley, E.C. (Ed.), The Unity of Evolutionary Biology, Portland, OR: Proceedings of the Fourth International Congress of Systematic and Evolutionary Biology, vol. 1. Dioscorides Press, pp. 380e395. Pavan, M., 1944. Considerazioni sui concetti di troglobio, troglofilo e troglosseno. Le Grotte d’Italia, ser 2 5, 35e41. Peck, S.B., 1990. Eyeless arthropods on the Galapagos Islands, Equador: composition and origin of the crtyptozoic fauna of a young, tropical, oceanic archipelago. Biotropica 22, 366e381. Peck, S.B., 2002. Florida and Caribbean karsts: an overview of diversity and origins of the obligate invertebrate cave faunas. In: Martin, J.B., Wicks, C.M., Sasowsky, I.D. (Eds.), Hydrogeology and Biology of Post-Paleozoic Carbonate. Karst Waters Special Publication 7 Aquifers. Karst Waters Institute, Charles Town, WV, pp. 54e60. Peck, S.B., Finston, T.L., 1993. Galapagos Islands troglobites: the questions of tropical troglobites, parapatric distributions with the eyed sister-species, and their origin by parapatric speciation. Mémoires de Biospéologie 20, 19e37. Peralta-Maraver, I., Galloway, J., Posselt, M., Arnon, S., Reiss, J., Lewandowski, J., Robertson, A.L., 2018. Environmental filtering and community delineation in the streambed ecotone. Scientific Reports 8, 15871. Pipan, T., Culver, D.C., 2012. Convergence and divergence in the subterranean realm: a reassessment. Biological Journal of the Linnean Society 107, 1e14. Plath, M., Tobler, M., 2010. Subterranean fishes of Mexico (Poecilia mexicana, Poeciliidae). In: Trajano, E., Bichuette, M.E., Kapoor, B.G. (Eds.), Biology of Subterranean Fishes. Science Publishers, Enfield, NH, pp. 281e330. Poulson, T.L., 1963. Cave adaptation in amblyopsid fishes. The American Midland Naturalist 70, 257e290. Pulliam, H.R., 1988. Sources, sinks, and population regulation. The American Naturalist 132, 652e661. Racovitza, E.G., 1907. Essai sur les problèmes biospéologiques. Archives de Zoologie Expérimentale et Générale 6, 371e488. Ribera, I., Cieslak, A., Faille, A., Fresneda, J., 2018. Historical and ecological factors determining cave diversity. In: Moldovan, O.T., Kovac, L., Halse, S. (Eds.), Cave Ecology. Springer Nature, Cham, Switzerland, pp. 229e254. Riesch, R., Plath, M., Schlupp, I., 2011. Speciation in caves: experimental evidence that permanent darkness promotes reproductive isolation. Biology Letters 7, 909e912. Romero, A., 2009. Cave Biology. Life in Darkness. Cambridge University Press, Cambridge. Romero, A., Green, S.M., 2005. The end of regressive evolution: examining and interpreting the evidence from cave fishes. Journal of Fish Biology 67, 3e32. Rosa, G., Penado, A., 2013. Rana iberica (Boulenger, 1879) goes underground: subterranean habitat usage and new insights on natural history. Subterranean Biology 11, 15e29.

I. Setting the scene: groundwater as ecosystems

110

4. Ecological and evolutionary jargon in subterranean biology

Schiner, J.R., 1854. Fauna der Adelsberger-, Luegger-, and Magdalenen Grotte. In: Schmidl, A. (Ed.), Die Grotten und Höhlen von Adelsberg, Lueg, Planina und Laas. Braunmü, Wien, pp. 231e272. Schiødte, J.C., 1849. Bidrag til den underjordisje Fauna. In: Transactions of the Royal Danish Society. 5th ser, Division of Natural History and Mathematics, vol. 2, pp. 1e39. Schluter, D., 2001. Ecology and the origin of species. Trends in Ecology & Evolution 16, 372e380. Schluter, D., 2009. Evidence for ecological speciation and its alternative. Science 323, 737e741. Schilthuizen, M., Cabanban, A.S., Haase, M., 2005. Possible speciation with gene flow in tropical cave snails. Journal of Zoological Systematics and Evolutionary Research 43, 133e138. Simcic, T., Sket, B., 2019. Comparison of some epigean and troglobitic animals regarding their metabolism intensity. Examination of a classical assertion. International Journal of Speleology 48, 133e144. Skeels, A., Cardillo, M., 2019. Reconstructing the geography of speciation from contemporary biodiversity data. The American Naturalist 193, 240e255. Sket, B., 2008. Can we agree on an ecological classification of subterranean animals? Journal of Natural History 42, 1549e1563. Stanford, J.A., Gaufin, A.R., 1974. Hyporheic communities of two Montana rivers. Science 185, 700e702. Stoch, F., 2004. Colonization. In: Gunn, J. (Ed.), Encyclopedia of Caves and Karst Science. Taylor & Francis, Inc, New York, USA, pp. 483e488. Tobin, B.W., Hutchins, B.T., Schwartz, B.F., 2013. Spatial and temporal changes in invertebrate assemblage structure from entrance to deep-cave zone of a temperate marble cave. International Journal of Speleology 42, 203e214. Tobler, M., 2009. Does a predatory insect contribute to the divergence between cave- and surface-adapted fish populations? Biology Letters 5, 506e509. Tobler, M., Riesch, R., Tobler, C.M., Schulz-Mirbach, T., Plath, M., 2009. Natural and sexual selection against immigrants maintains differentiation among micro-allopatric populations. Journal of Evolutionary Biology 22, 2298e2304. Trajano, E., 2012. Ecological classification of subterranean organisms. In: White, W.B., Culver, D.C. (Eds.), Encyclopedia of Caves, second ed. Academic/Elsevier Press, Amsterdam, pp. 275e277. Trajano, E., de Carvalho, M.R., 2017. Towards a biologically meaningful classification of subterranean organisms: a critical analysis of the Schiner-Racovitza system from a historical perspective, difficulties of its application and implications for conservation. Subterranean Biology 22, 1e26. Trontelj, P., 2018. Structure and genetics of cave populations. In: Moldovan, O.T., Kovác, L., Halse, S. (Eds.), Cave Ecology. Springer, Cham, pp. 269e295. Trontelj, P., 2019. Adaptation and natural selection in caves. In: White, W.B., Culver, D.C., Pipan, T. (Eds.), Encyclopedia of Caves. Elsevier/Academic Press, Amsterdam, pp. 40e46. Trontelj, P., Blejec, A., Fiser, C., 2012. Ecomorphological convergence in cave communities. Evolution 66, 3852e3865. Vandel, A., 1964. Biospéologie: la biologie des animaux cavernicoles. Gauthier-Villars, Paris. Via, S., 2001. Sympatric speciation in animals: the ugly duckling grows up. Trends in Ecology & Evolution 16, 381e390. Ward, J.V., Voelz, N.J., 1997. Interstitial fauna along an epigean-hypogean gradient in a Rocky Mountain river. In: Gibert, J., Mathieu, J., Fournier, F. (Eds.), Groundwater/surface Water Ecotones: Biological and Hydrological Interactions and Management Options. Cambridge University Press, Cambridge, pp. 37e41. White, M.J.D., 1978. Modes of Speciation. W. H. Freeman and Company, San Francisco. Wilkens, H., Hüppop, K., 1986. Sympatric speciation in cave fishes? Studies on a mixed population of epi- and hypogean Astyanax (Characidae, Pisces). Journal of Zoological Systematics and Evolutionary Research 24 (3), 223e230. Wilkens, H., Strecker, U., 2017. Evolution in the Dark. Darwin’s Loss Without Selection. Springer, Cham.

I. Setting the scene: groundwater as ecosystems

S E C T I O N I I

Drivers and patterns of groundwater biodiversity

This page intentionally left blank

C H A P T E R

5 Groundwater biodiversity and constraints to biological distribution Pierre Marmonier1, Diana Maria Paola Galassi2, Kathryn Korbel3, Murray Close4, Thibault Datry5 and Clemens Karwautz6 1

Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR 5023 LEHNA, Villeurbanne, France; 2Department of Life, Health and Environmental Sciences, University of L’Aquila, L’Aquila, Italy; 3School of Natural Sciences, Macquarie University, Sydney, Australia; 4Institute of Environmental Science and Research, Christchurch, Canterbury, New Zealand; 5INRAE, UR-RiverLY, Lyon, France; 6University of Vienna, Department of Functional & Evolutionary Ecology, Vienna, Austria

Introduction Groundwater biodiversity is invisible to most people outside the field of groundwater ecology. Media typically convey the idea of subterranean life being restricted to a few hyper-specialized creatures. In fact, microbes densely colonize groundwater and even metazoans are many and show varying degrees of specialization. The first mentions of blind and depigmented groundwater metazoans probably date back to the report in 1541 of the Chinese hyaline fish Sinocyclocheilus hyalinus (see Romero, 2001), followed by the report of the European cave salamander, Proteus anguinus, in 1689 (Aljancic et al., 1993). With microorganisms, already Antonie van Leeuwenhoek (1677) discovered bacteria in the water of large wells and later, Hassall (1850) reported on microbes in a London waterwork. Since the first discoveries of living organisms in groundwater, knowledge of groundwater biodiversity has increased worldwide (Griebler and Lueders, 2009; Zagmajster et al., 2018; Niemiller et al., 2019). Today, we know that obligate groundwater organisms represent an important, yet largely underestimated, component of the Earth’s total biological diversity (Culver and Holsinger, 1992; Danielopol et al., 2000; Malard, 2022). The difficulty in assessing the true diversity of groundwater life is primarily due to a low sampling effort. Groundwater represents the

Groundwater Ecology and Evolution, Second Edition https://doi.org/10.1016/B978-0-12-819119-4.00003-2

113

© 2023 Elsevier Inc. All rights reserved.

114

5. Groundwater biodiversity and constraints to biological distribution

largest reservoir of liquid freshwater on Earth, but groundwater ecologists have only explored a minor fraction of it. Groundwater metazoan communities comprise a mix of species that show different degrees of dependence on the subterranean environment. In the first edition of the Groundwater Ecology textbook, Gibert et al. (1994a) recognized three main ecological categories: stygoxenes, stygophiles, and stygobionts. Stygoxenes have no affinities with groundwater: they occur accidently in aquifers. Stygophiles are represented by a variety of metazoans that all have higher affinities for the groundwater environment than do stygoxenes. They include insect species whose early instar larvae can reside in the subsurface sediments of surface streams as well as species with a life cycle necessitating both a groundwater and surface water stage (for example the stonefly Isocapnia) or those that retreat to groundwater in times of stress (e.g., prolonged drought). Stygophiles are also represented by species with no aerial stage that can complete their entire life cycle either in surface water or in groundwater (for example some nematodes, oligochaete worms, crustaceans, and tardigrades). Stygobionts are obligate groundwater species that complete their entire life cycle exclusively in groundwater. Culver and his coauthors (this volume) question the need and justification for such an elaborated ecological classification and terminology of groundwater metazoans. They prefer to use the general terms of specialist and generalist species. Specialist groundwater species have a strict dependence on groundwater because they complete their entire life cycle exclusively in groundwater (stygobionts) or because they necessarily complete a part of their life cycle there. Generalist species exploit a wide range of resources that they can draw from both groundwater and surface water. The three ecological categories described above do not apply well to microorganisms. Microbes are continuously imported into the subsurface by surface water infiltrating into aquifers. Only a minute fraction of the cells in pore water seem well adapted to the environmental conditions and is highly active. The active part of groundwater microbial communities is attached to the rocks and sediment matrix as single cells, small colonies, and in exceptional cases as a surface covering biofilm (Griebler et al., 2022). Only zones that are hydrologically isolated from the surface for hundreds and thousands of years, may harbor strains not found anywhere else. In general, the groups of microorganisms found in groundwater do not contain endemic taxa but are known already from soils and surface waters (Griebler and Lueders, 2009; Fillinger et al., this volume). The diversity of obligate groundwater organisms is unevenly distributed across taxa. Some metazoan groups, particularly within the hexapods, show very few species in groundwater, whereas other groups, particularly within the crustaceans, are more diversified in groundwater than in surface water. In Europe, the number of obligate groundwater crustaceans exceeds the number of surface-dwelling crustacean species, even though the description of groundwater species lags behind that of surface species (Stoch and Galassi, 2010). As a rule of thumb, the obligate groundwater fauna is taxonomically dominated by crustaceans, followed by molluscs and oligochaete worms. An extensive survey of stygobionts in six European countries - Belgium, France, Italy, Portugal, Slovenia, and Spaind showed that crustaceans, molluscs, and oligochaete worms represented 70%, 16%, and 6.1% of the obligate-groundwater species diversity (Deharveng et al., 2009; Venarsky et al., chapter 10, this volume). However, these proportions vary across continents. In Europe, only two species of stygobiotic insects, belonging to the dytiscid beetles, have been discovered, whereas over 100 species of stygobiotic dytiscid species have been described from calcrete aquifers in Australia (Langille et al., 2021). II. Drivers and patterns of groundwater biodiversity

An overview of groundwater biodiversity

115

Groundwater organisms are likely to be found wherever there are open spaces within the water-filled subterranean rock and sediment matrix and a reconcilable temperature prevails. Some species make use of the food resources available in superficial twilight habitats (Culver and Pipan, 2014), whereas others colonized habitats at considerable depths below the water table: 500 m in lakes, 600 m in wells, and 3600 m in mines (Fiser et al., 2014). In all cases, microbes are found in even deeper zones (Pedersen, 2000), with their abundance and distribution mainly governed by the availability of energy and temperature (Griebler and Lueders, 2009). The diversity and abundance of obligate groundwater metazoan assemblages are spatially heterogeneous at local (Malard et al., 2002; Gutjahr et al., 2014), regional (Johns et al., 2015) and continental scales (Eme et al., 2015; Iannella et al., 2020, 2021). Striking features in the spatial distribution of groundwater metazoans are described in the next chapter of this book (Zagmajster et al., this volume). In this chapter, we provide a brief account of the taxonomic diversity of living forms in groundwater including viruses, prokaryotes, microeukaryotes, and metazoans. Then, we present the main constraints to biological distributions in groundwater. Emphasis is put on the diversity and constraints to the distribution of metazoans since another chapter of this book is dedicated to microbial diversity and processes in groundwater (Fillinger et al., this volume). For sake of clarity, we separately consider physical and chemical constraints and biotic interactions. However, we acknowledge that these constraints interact across all ranges of spatial and temporal scales to produce complex distribution patterns (see Gibert et al., 1994a for a discussion of scales, hierarchy, and processes in groundwater ecology). Among physical constraints, we focus on the importance of the size and connectedness of voids, hydrological exchanges between groundwater and surface water, groundwater chemistry, and temperature. Then, we provide examples of how competition, predation, and other forms of biotic interactions may affect the distribution of organisms. We end this chapter by considering how the effects of past constraints linked to major paleogeographic events and historical climates have left their imprints on the present-day distribution patterns of groundwater biodiversity.

An overview of groundwater biodiversity All groundwater ecosystems are characterized by the absence of light; hence, they lack photosynthetic primary production. In the absence of light-driven production, particulate organic carbon production at the base of groundwater food webs essentially comes from two pathways: chemoautotrophic primary production, where bacteria fix inorganic carbon to produce biomass, and heterotrophic production, where bacteria produce biomass from assimilation of dissolved organic compounds, which are mainly imported from surface environments. Most groundwater food webs are mainly supported by heterotrophic production (Simon, 2019). Shallow subterranean habitats and deep habitats directly connected to the surface by conduit flow may receive appreciable amounts of organic matter (OM) from the surface. However, heterotrophic production is severely limited in many groundwater systems because a substantial fraction of OM produced at the surface is intercepted in the soil layers and the vadose zone. Datry et al. (2005) estimated that the annual flux of dissolved organic carbon (DOC) reaching the water table of an unconsolidated sediment aquifer was one to two

II. Drivers and patterns of groundwater biodiversity

116

5. Groundwater biodiversity and constraints to biological distribution

orders of magnitude lower than the annual flux of DOC in the soil organic layer. Herrmann et al. (2020) provided evidence that the importance of microbial biomass produced by chemolithoautotrophs relative to that of heterotrophs might be seriously underestimated. In any way, quantitative data on organic carbon import to the subsurface as well as rates of chemoautotrophic inorganic carbon fixation are lacking (Griebler et al., 2022). Although low food availability ranks most groundwater habitats among the most energylimited habitats on Earth, they nevertheless support a high diversity of living forms occupying a reduced number of levels in the trophic cascade (Gibert and Deharveng, 2002). Chemolithoautotrophic bacteria act as primary producers, heterotrophic bacteria and fungi as primary consumers, whereas protozoans and metazoans, including invertebrates, fish and salamanders, occupy the higher trophic levels (Herrmann et al., 2020; Griebler et al., 2022; Venarsky et al., chapter 10, this volume). Below, we provide a brief overview of the current knowledge of the diversity of living forms in groundwater.

Viruses While it is widely accepted that microbes occupy almost every corner on this planet, including groundwater and the deep terrestrial subsurface (Griebler and Lueders, 2009), it has been overlooked for a long time that whenever there are microbes there are viruses. The vast majority of viruses in natural ecosystems infect prokaryotes (i.e., Bacteria and Archaea; see below). These viruses we call (bacterio) phages. Phages are the most abundant biological entities in the biosphere (Suttle, 2005). Unfortunately, almost nothing is known about phages in groundwater. On one hand, recent estimates indicate that >80% of all prokaryotic biomass on Earth is located in the subsurface (e.g., terrestrial aquifers, vadose zones, and below the seafloor; Bar-On et al., 2018). On the other hand, as has been mentioned already above, groundwater ecosystems are typically energy poor exhibiting comparatively low productivity, which results in low concentrations and activity of prokaryotes, the predominant hosts of viruses in groundwater. The abundance of phages in aquatic environments is generally higher than the number of prokaryotes with a virus-to-prokaryote ratio (VPR) of 10 reported frequently. Considering all available data, the VPR in groundwater ranges between 0.08 and 728, with the majority of studies reporting values < 10 (Schweichhart et al., 2022). While there is a handful of studies that quantified virus abundance in groundwater, viral diversity is untapped. One study in granitic groundwater observed phages down to a depth of 450 m and found a diverse set of viral morphotypes resembling tailed phages, polyhedral phages, filamentous phages, and fusiform archaeal phages (Kyle et al., 2008). To date, only a few phages have been isolated from groundwater microbes (Eydal et al., 2009; Hylling et al., 2020). Metagenomics is the tool of choice for characterizing viruses because they do not share a conserved gene that could be used for phylogenetic analysis and taxonomic classification. Besides the presence of families commonly occurring in surface waters, i.e., Myoviridae , Podoviridae , Siphoviridae , other groups have been particularly detected in groundwater, i.e., Microviridae and Inoviridae (Smith et al., 2013; Roux et al., 2019). The functional role of these phages has not been explored, however, an intimate involvement in microbial food web interactions and carbon flow is expected (Schweichhart et al., 2022).

II. Drivers and patterns of groundwater biodiversity

An overview of groundwater biodiversity

117

Prokaryotes: Archaea and Bacteria The majority of the Earth’s prokaryotic biomass is located in the subsurface (Bar-On et al., 2018). Prokaryotic communities not only represent the major fraction of total biomass in groundwater, they are also exceptional in their taxonomic and functional diversity. The presence of a diverse and abundant prokaryotic community in groundwater has been known for a long time (van Leeuwenhoek 1677; Hvid-Hansen, 1951). In the past decades, research indicating that microbes are present even in the most extreme subterranean ecosystems (e.g., volcanic groundwater-fed springs, Segawa et al., 2015; Bornemann et al., 2022) and at depths of 1000s of meters below the soil surface have shifted the perspective on the limits of life (Pedersen, 2000; Newman and Banfield, 2002). Prokaryotic groundwater communities play a central role in the cycling of nitrogen, carbon, sulfur, and iron within aquifers (Fillinger et al., this volume). Compared to surface waters, the densities of prokaryotes are much lower in the subsurface. They typically range from 104 to 108 cells gram
1 of sediment and 103 to 105 cells mL
1 of groundwater (Griebler and Lueders, 2009). The majority of groundwater bacteria are attached rather than free-living, with suspended bacteria only contributing to 10% of the total prokaryotic biomass (Smith et al., 2018). Attached bacteria occur predominantly in small, unevenly distributed colonies rather than large biofilms (Smith et al., 2018). Due to the sampling limitations of subsurface sediments, the majority of research data on microbial groundwater communities is attained from pumped water samples (Griebler et al., 2022). Prokaryotic communities in shallow aquifers with high connectivity to the surface are more dynamic in their composition and more active than communities in deeper aquifers. However, the strong heterogeneity within and among aquifers as well as methodological limitations complicate attempts to summarize the overall diversity of groundwater microbes. Today, the characterization of the prokaryotic diversity in aquifers is largely based on 16S rDNA amplicon sequencing data. Taxa that are commonly identified in groundwater include a mixture of bacteria and archaea that do not seem to be exclusive to the subsurface (Griebler and Lueders, 2009). Deep groundwater aquifers tend to have fewer and less diverse communities, commonly containing substantial proportions of methanogens, sulfate-reducing bacteria, thermophilic prokaryotes, and an increased archaeal abundance (Purkamo et al., 2018). The most abundant bacteria in aquifers are found within the bacterial lineages of Alphaproteobacteria, Gammaproteobacteria, Betaproteobacteria, Flavobacteriia, Actinobacteria, Sphingobacteria, and Bacilli. Environmental parameters such as temperature, pH, and nutrient supply, influence microbial community composition (Stegen et al., 2018; Fillinger et al., 2019a), but microscale conditions (e.g., redox processes) are highly relevant for the activity of cells (Peiffer et al., 2021). The array of functions within groundwater prokaryotes spans almost all electron acceptors and donors that provide enough energy to survive. Specific processes and model organisms have been studied in great detail such as sulfate reduction (e.g., Desulfobacterales), denitrification (e.g., Pseudomonadales), ammonia oxidation by bacteria (e.g., Nitrosomondales), and archaea (e.g., Nitrosopumilales), iron reduction (Desulfuromondales: Geobacter) and methanogenesis (e.g., Methanosarcinales). Recently, a combination of high-resolution electron microscopy and molecular techni ques revealed an even more diverse and previously unknown community of prokaryotic cells

II. Drivers and patterns of groundwater biodiversity

118

5. Groundwater biodiversity and constraints to biological distribution

- many of which are smaller than 0.2 mm and lack several biosynthetic pathways (Luef et al., 2015; He et al., 2021). Metagenomic data highlight the importance of species interactions and metabolic handoff (e.g., one microbe’s waste is another microbe’s food) in the subsurface (Anantharaman et al., 2016; Hug and Co, 2018). Many of these newly discovered prokaryotes belong to the candidate phyla radiation (CPR) group, which are difficult to be cultivated and are even missed by the classic 16S rRNA approach. Many of the CPR bacteria live as obligate symbionts or parasites (Chaudhari et al., 2021; He et al., 2021). The superphyla Patescibacteria and DPANN archaea (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaeota) are representative of this lifestyle.

Microeukaryotes Single-cell eukaryotic microorganisms, including groups commonly referred to as fungi and protozoa, play an important role in soils and surface aquatic systems. Their diversity, functions, and implication in groundwater food webs are increasingly being targeted by the use of novel sequencing technologies (Sohlberg et al., 2015; Korbel et al., 2017; Perkins et al., 2019; Herrmann et al., 2020; Retter and Nawaz, 2022). Although microeukaryotes are less abundant and diverse in groundwater communities than representatives of the Bacteria and Archaea (Griebler and Lueders, 2009), they substantially contribute to the diversity of microbial communities. Owing to their diverse life strategies as decomposers, symbionts, parasites, and pathogens, fungi, similar to the prokaryotes, play vital ecological roles in aquatic environments. While the functional importance of fungi in surface waters is long appreciated, i.e., the quantitative contribution to leave litter breakdown in streams, their taxonomic diversity has been historically understudied (Grossart et al., 2019). The reasons are manifold. Reproduction life cycles in which fungi produce distinct fruiting bodies are often unnoticed. There are biases in the molecular analysis due to the choice of inappropriate primers and DNA barcode markers. Finally, only a few aquatic ecosystems have been systematically investigated for fungi. Thus, it is not surprising that there are only a few studies conducted on fungi in groundwater (Retter and Nawaz, 2022). Fungi in groundwater habitats so far are mostly affiliated with pathogenic and/or saprotrophic lineages. Early phylogenetically diverging lineages include Cryptomycota and Microsporidia of which many are endoparasites (Livermore and Mattes, 2013). Members of another ancient branch of fungi comprise chytrids and blastocladiomycetes. Nawaz et al. (2018) reported the Chytridiomycota fraction to make up the third-largest phylum detected in their groundwater study. In groundwater, chytrids are mainly parasites of other fungi or invertebrates (Grabner et al., 2020). Wurzbacher et al. (2020) found that around 8% of the fungal diversity recovered from volcanic springs was made up of early diverging lineages of fungi, with a significant part belonging to yet unexplored yeast lineages. Most sequences recovered from groundwater metabarcoding efforts are affiliated with Dikarya (Ascomycota þ Basidiomycota), many of them yeasts or yeast-like taxa. Yeast species are all placed within Dikarya but do not form a monophyletic group. Yeasts are especially remarkable, as they could be recovered from every habitat of the world, including the deep subsurface (Sohlber et al., 2015; Ivarsson et al., 2018; Purkamo et al., 2018). Dikarya grows on all kinds of organic substrates, such as carbohydrates, some being able to act well under

II. Drivers and patterns of groundwater biodiversity

An overview of groundwater biodiversity

119

oxygen-deprived conditions (facultative anaerobes). Lategan et al. (2012) identified 89 fungal strains in unconsolidated sediment aquifers of New South Wales, Australia. Fungi and yeasts represented 0) Open framework gravel (103 < k < 104 m/d)

Clay-bound gravel (k ~10-2 m/d)

D

Downwelling zone Upwelling zone

FIGURE 5.2 (A) Sediment heterogeneity in alluvial systems showing the example of four hydrofacies with contrasted void/grain (pore) sizes and values of permeability (k in m/day; photo by M. Close). (B) Location of downwelling and upwelling zones along a stream riffle showing measurements of vertical hydraulic gradients (VHG) in piezometers. (C) Physical clogging of sediment by deposition and infiltration of fine mineral particles (black dots). (D) Biological clogging of sediment by overgrowth of bacterial biofilm (gray layers around sand grains).

II. Drivers and patterns of groundwater biodiversity

124

5. Groundwater biodiversity and constraints to biological distribution

deposition, accumulation, and infiltration of fine sediments into the bed sediment of streams (Fig. 5.2C). This definition underestimates the role of the surface algal mat and interstitial bacterial communities that contribute to the clogging through proliferation and overgrowth (Fig. 5.2D; Marmonier et al., 2004). In its early stages, clogging generates anaerobic microenvironments and increases the surface available to biofilm, thereby potentially increasing the functional diversity of microbes. In its later stages, the complete filling of pores with fine sediments impedes interstitial water flow, generates steep vertical gradients in biogeochemical processes, and restricts the use of hyporheic sediments by surface aquatic taxa, especially fish larvae, large benthic insect larvae (Descloux et al., 2013) and macro-crustaceans (Mathers et al., 2014). Karst systems also show strong spatial heterogeneities in the size and connectivity of fractures. Beyond cave streams and large phreatic conduits that can harbor large-sized organisms, are small-size fissures through which move organisms, energy, and matter (Simon, 2019). As in alluvial systems, the distribution and dynamics of metazoan communities largely depend on the distribution and connection of groundwater flow between the conductive fractures (i.e., the equivalent of OFG in alluvial aquifers) and adjacent thinly fissured matrix of the saturated zone (Gibert et al., 1994b; Di Lorenzo et al., 2018). In the Lez Karst system, France, Malard et al. (1996) showed that wells separated by distances of only a few meters had contrasted metazoan community composition depending on the size, hydraulic conductivity, and surface hydrological connections of water-bearing fractures intersected by the wells. The fauna of the epikarst aquifer provides an example of species-rich communities dominated by small-sized organisms, including many copepods (Pipan and Culver, 2007).

Hydrological connection to the surface environment The degree of hydrological connection of subsurface habitats to the surface environment is a key parameter controlling the distribution of organisms in alluvial and karst aquifers (Hahn and Fuchs, 2009; Hermann et al., 2020). Aquatic subterranean habitats that exhibit a strong hydrological connection to the surface show increased temporal variability, higher fluxes of nutrients, OM, and dissolved oxygen, and are prone to the import of microorganisms with infiltrating surface water, as well as to colonization by aquatic surface metazoans. In river alluvial aquifers, the strength and direction of hydrological exchanges between the river and interstitial water are assessed by measuring the vertical hydraulic gradient (VHG) defined as the difference in height (cm) between the surface water level and the hyporheic water level (Baxter et al., 2003) (Fig. 5.2B). A negative VHG reflects the infiltration of surface water into the riverbed sediments (downwelling zones; Hendricks and White, 1991) that results in sediment patches characterized by elevated concentrations of biodegradable OM and higher densities of benthic organisms. A positive VHG reflects the exfiltration of groundwater into the riverbed (upwelling zones), which results in oligotrophic sediment patches characterized by constant temperature and higher densities of obligate groundwater organisms (DoleOlivier and Marmonier, 1992; Brunke and Gonser, 1999; Korbel et al., 2022). Spatial variation in the infiltration of surface water also drives community composition in karst aquifers (Gibert et al., 1994b). In the Foussoubie karst system, France, subsurface habitats fed by sinking surface streams were dominated by surface organisms (e.g., Ephemeroptera, Diptera

II. Drivers and patterns of groundwater biodiversity

Chemical constraints to biological distribution

125

Chironomidae, and Cladocera), whereas karstic springs fed by diffuse infiltration of rainwater were dominated by stygobionts (e.g., Niphargus virei, Acanthocyclops venustus; Vervier and Gibert, 1991).

Temperature Subsurface habitats are among the most thermally stable habitats on Earth. Temperature seasonality of groundwater decreases with increasing depth below the soil surface until the temperature becomes constant throughout the year at a depth of w10e20 m. Temperate caves also show steep gradients in air temperature seasonality from the outer (annual temperature variation similar to the outside) to the inner passages (annual variation few tenths of degrees) (Mammola et al., 2019a). The climatic variability hypothesis predicts that species living in a thermally buffered environment should have reduced thermal tolerance breadth (Stevens, 1989). In agreement with theory, studies performed using subterranean terrestrial arthropods showed that specialization in deep subterranean life involved a reduction in thermal tolerance (Mammola et al., 2019a; Colado et al., 2022). The lower thermal tolerance among specialized subterranean terrestrial taxa may in turn constrain the size of their geographic and elevation ranges because dispersers are more likely to encounter temperatures outside their thermal tolerance. A formal test of the climatic variability hypothesis is lacking for groundwater taxa but preliminary data suggest that their thermal niche breadth correlates with the range of temperatures they encounter in their geographic range (Mermillod et al., 2013). Nevertheless, there is substantial variation in the thermal niche features among groundwater taxa (Eme et al., 2014; Di Lorenzo and Galassi, 2017; Castaño-Sánchez et al., 2020a). Similar to metazoans, microbial species do show a specific thermal optimum and tolerance. Groundwater ecosystems are typically inhabited by psychrophilic and mesophilic microbes. Groundwater temperature changes were shown to affect biodiversity (Brielmann et al., 2009; Griebler et al., 2016). Understanding groundwater temperature variation and its causes are key to assessing the differential ability of groundwater species to cope with anthropogenic warming of groundwater (e.g., due to geothermal energy use) and global warming (Griebler et al., 2016; Retter et al., 2020; Becher et al., 2022).

Chemical constraints to biological distribution Groundwater chemistry Groundwater chemical characteristics are determined by the lithology of the aquifer, solution kinetics, and flow patterns, as well as by natural or artificial recharge of groundwater with surface water (Foulquier et al., 2011). While groundwater composition does play an important role in the diversity and distribution of microorganisms, it is often difficult, at regional scales, to disentangle the relative influence of water chemistry from the physical features of habitats on the diversity of groundwater metazoan communities. Indeed, water chemistry and habitat feature both covary with the lithology and hydrodynamics of aquifers. Aquifers in carbonated rocks have both water with higher dissolved solid content and larger void size than aquifers in metamorphic rocks. However, physical habitat features explained a

II. Drivers and patterns of groundwater biodiversity

126

5. Groundwater biodiversity and constraints to biological distribution

greater proportion of variation in metazoan community than groundwater chemistry in most regional-scale studies (Dole-Olivier et al., 2009; Hahn and Fuchs, 2009; Johns et al., 2015; Korbel and Hose, 2015). Human activities also cause major changes in the chemistry of groundwater by introducing pollutants that may affect the growth and survival of groundwater microorganisms and metazoans (Castaño-Sánchez et al., 2020b; Becher et al., 2022, Fillinger et al., this volume). However, in the present section, we restrict ourselves to biological constraints imposed by natural variation in groundwater chemistry: the tolerance of groundwater organisms to chemical polutants is presented by Di Lorenzo et al. (this volume). Temporal and spatial changes in dissolved ions represent a stress for metazoans because they imply an osmoregulation activity, which is energetically expensive (Brooks and Mills, 2011). A major ion such as calcium is essential for molluscs and crustaceans because it controls the shell or exoskeleton development and the rate of molting (Rukke, 2002). However, groundwater metazoans appear to tolerate a wide range of total dissolved solids (i.e., the sum of dissolved salt content). Acute toxicity tests performed using a number of freshwater stygobiotic crustaceans including harpacticoids, cyclopoids, syncarids, and asellid isopods reported LC50 values (lethal concentrations for 50% of the population at 96 h) ranging from 2.84 to 12.7 g NaCl/L (Castaño-Sánchez et al., 2020a, 2021). Diversified obligate groundwater communities of metazoans were collected in a broad range of habitats showing highly contrasted concentrations of total dissolved solids. These include the hyporheic zone of Alpine glacial rivers containing water with specific conductance 50%) (Juberthie et al., 1996), captive survival can be improved by providing optimal artificial conditions, as recently demonstrated in the tourist cave of Postojna (Bizjak-Mali et al., 2017). Detailed gonad morphology shows a positive correlation between body length and egg maturation, and the absence of seasonality of the process in females (Bizjak-Mali and Bulog, 2010; Bizjak-Mali, 2017). On the other hand, body size seems to be a poor predictor of the

IV. Principles of evolution in groundwater

316

13. The olm (Proteus anguinus), a flagship groundwater species

reproductive status of olm males, while spermatogenesis, which takes place in 2-year cycles, seems to be seasonal and occurs more frequently from late summer to mid-winter. Considering the stable conditions of subterranean groundwater habitats, the seasonality of spermatogenesis is surprising. The loose synchronicity in gametogenesis between the sexes clearly underlines our incomplete understanding of reproduction in this amphibian. Olms have a female-biased sex ratio of about two to one, and gonadal anomalies, such as a high proportion of degenerated (atretic) ovarian follicles, egg cells in testes (testis-ova) in w30% of the males examined, and hermaphroditism with apparently functional chimeric gonads with synchronously developing male and female gametocytes (Bizjak-Mali and Sessions, 2016; Bizjak-Mali, 2017). To our knowledge, this suite of reproductive peculiarities has not been reported for any other cave-dwelling vertebrate. The proximate mechanism of both the sex ratio and gonad anomalies is not known, but might be related to recently reported cytogenetic evidence of an X/Y sex chromosome translocation (Sessions et al., 2016), which is responsible for homomorphic male and female karyotypes (Fig. 13.5). Both genera of the family Proteidae, Proteus and Necturus, are characterized by 19 pairs of chromosomes, a chromosome number that is unique among salamander families (Sessions, 2008). Unlike Proteus, all species of the genus Necturus have strongly differentiated heteromorphic X/Y sex chromosomes (Fig. 13.5) (Sessions and Wiley, 1985). The translocation in the olm renders sex identification impossible even at the level of chromosomes. Such a translocation can disrupt the function of genes involved in sex determination through random “position effects” with reproductive consequences such as the observed intersexes and hermaphrodites. The apparently negative reproductive consequences of such a chromosomal rearrangement suggests that it may have some other biological significance, perhaps related to cave adaptations, a possibility that is currently under investigation.

FIGURE 13.5 Idiograms of both genera of the family Proteidae, Proteus and Necturus, with a distinctive Cbanding pattern of heterochromatin at the end of the long arms of Proteus chromosome one corresponding to the pattern on Y chromosome of Necturus. Modified from Sessions et al. (2016).

IV. Principles of evolution in groundwater

The overlooked part of groundwater ecology: symbioses, pathogens and parasites

317

The overlooked part of groundwater ecology: symbioses, pathogens and parasites Apart from the recognized role of the olm as the top predator of subterranean waters of the Dinaric karst, several aspects of its ecology, including interactions with microorganisms and parasites, remain understudied. The inaccessibility of a considerable part of the underground environment, the relative scarcity of biological material and the limited taxonomic knowledge of researchers in the past are reflected in sporadic and often generalized descriptions of olm’s parasites and symbionts. The only two attempts of comprehensive coverage of interactions with other organisms include the work on the parasites of subterranean organisms dating back more than half a century (Vandel, 1965), and a brief overview of the parasites of the olm (Kostanjsek et al., 2017). Among the specialized parasites described in the olm are the Myxozoan Chloromyxum protei, which inhabits its renal ducts (Joseph, 1905), the trematode Plagioporus protei (Prudhoe, 1945), which colonizes the small intestine, and a more recent description of the thornyheaded worm Acantocephalus anguillae balcanicus, which infests the intestinal wall and various other organs in the body cavity of the olm (Amin et al., 2019) (Fig. 13.6A). The digestive tract and peritoneal cavity of the olm are frequently colonized by nematodes (Bizjak-Mali and Bulog, 2004). Although the first attempts of scientific classification of nematodes in the olm (e.g., Nematoideum protei anguinii) were made as early as the beginning of the 19th century (Rudolphi, 1819), their taxonomic position remains unclear. In addition to free-living nematodes, which occasionally colonize the intestine and even the body cavity (Fig. 13.6E), encysted nematodes entrapped in spherical formations in the wall of the pancreas and duodenum (Fig. 13.6C and D), occur as common parasites of olm’s digestive system (Schreiber, 1933). Other less specific records of parasites include unidentified adult trematodes in the gut (Matjasic, 1956) and monogenean flatworms on the skin and gills of the black olms, and recently also white morph. Besides the parasites, ubiquitous protozoa, including amebae and ciliates from the genera Trichodina and Vorticella, occasionally colonize the skin as epibionts. The accessibility of high-throughput DNA sequencing technologies over the last decade has significantly improved our knowledge of the importance of skin-associated microbial communities as a source of metabolic capabilities and protection against pathogens in amphibians. Recent threats to amphibian diversity from emerging pathogens, the general lack of information on skin microbiota in neotenic amphibians and conservation potentials initiated the study of the composition and potential role of skin bacteria in olm. Next generation sequencing analysis of skin bacterial communities in individuals from five different genetic lineages of olms and their aquatic environment revealed the environmental origin of skin bacteria. Rather than simply reflecting the bacterial community in the surrounding water, the bacteria colonizing the skin of analyzed individuals consisted of resident microbial community dominated by five bacterial taxa, indicating the selective pressure of the skin environment on colonizing bacteria (Kostanjsek et al., 2019). The high similarity of the resident skin bacteriome between individuals from different unpolluted sampling sites and the replacement of a significant proportion of the resident microbiota by Enterobacteria detected in individuals exposed to pollution from wastewater and agriculture (Fig. 13.7.)

IV. Principles of evolution in groundwater

318

13. The olm (Proteus anguinus), a flagship groundwater species

FIGURE 13.6 Panel summarizing main known parasites and pathogens of olm. (A) Two adult individuals of Acanthocephalus anguillae balcanicus from the olm’s gut, and a detail of its hooked proboscis (inset); (B) Saprolegnia on the gills of the black morph (arrow) and Saprolegnia sp. isolate (inset); C) Nodular formations in the wall of small intestine (arrows) and (D) a section of individual nodule with nematodes (arrowheads); (E) Free-living nematode from the gut contents; (F) Electronic micrograph of Exophiala salmonis hyphae in a skin ulcer; (G) Skin hemorrhages on the head caused by Aeromonas infection.

demonstrates the potential of the resident skin microbiota to provide protection against invading microbes by occupying the niche. At the same time, the composition of the skin microbiota of olms could serve as an indicator of the status of environmental pressure and the well-being of the host.

IV. Principles of evolution in groundwater

The overlooked part of groundwater ecology: symbioses, pathogens and parasites

319

FIGURE 13.7 Relative abundance of prevailing bacterial families in the skin of Proteus anguinus individuals from different populations (Samples 1e7) and in cave water. Credit: Figure adapted from Kostanjsek et al. (2019).

Due to the inaccessibility of its natural habitat, individuals of P. anguinus are often kept in artificial or seminatural ex-situ environments for scientific purposes or recovery, breeding and for exhibitions. Despite the best efforts, the controlled conditions of the ex-situ environment can still cause stress to captive olms, often resulting in increased susceptibility to opportunistic microbial infections. Recorded opportunistic infections caused by fungi include oomycete water molds from the genus Saprolegnia sp., which infect the outer surface (Kogej, 1999; Lukac et al., 2019) (Fig. 13.6B), as the most common opportunistic infection of the olm, and skin lesions caused by the black yeast Exophiala salmonis (Bizjak-Mali et al., 2018) (Fig. 13.6F). Various fungi and oomycetes have also been identified in the outer coat of olm eggs laid in captivity (Zalar et al., 2016). The most common bacterial pathogen associated with opportunistic infections in the olm is Aeromonas hydrophila, which causes a systemic infection associated with cutaneous erythema and haemorrhagic changes in other tissues, and is commonly known as “red leg syndrome” (Densmore and Green, 2007; Lukac et al., 2019) (Fig. 13.6G). Well-being of captive animals and the establishment of a much-needed sustainable breeding program for olms depends heavily on providing ex-situ conditions closely mimicking the natural environment and on the detection and treatment of potential medical conditions of captive animals. To address the latter two issues, several diagnostic protocols have been developed in recent years, including monitoring of hematological parameters of olms (Gredar et al., 2018) and treatment of symptomatic individuals (Bizjak-Mali et al.,

IV. Principles of evolution in groundwater

320

13. The olm (Proteus anguinus), a flagship groundwater species

2018; Lukac et al., 2019). At the same time, a study is underway on possible monitoring of stress in captive animals by analysing changes in the composition of their cutaneous microbiota. Besides opportunistic infections and frequent amphibian diseases with bacterial etiology such as flavobacteriosis, mycobacteriosis and chlamydiosis (Densmore and Green, 2007), newly emerging pathogens pose further microbial threat to the olm. In particular, chytrid fungi of the genus Batrachochytrium and ranaviruses from the Iridioviridae family (Densmore and Green, 2007; Latney and Klaphake, 2013), which are responsible for the extinction of several hundred species of amphibians, causing a dramatic global decline in their diversity in recent decades (Scheele et al., 2019). Due to the high mortality and the rapid spread of these pathogens, their occurrence is monitored in amphibian populations throughout Central and Western Europe. Despite recently shown tolerance of the olm to Batrachochytrium salamandrivorans infection under laboratory conditions (Li et al., 2020) and the absence of chytrid fungi or ranaviruses in so far examined olm populations in Slovenia (Kostanjsek et al., 2021a) and Croatia (Lukac et al., 2019), continuous monitoring of these pathogens in surface and subterranean amphibians should be established, as their introduction to underground water systems of the Dinaric Karst still poses a considerable threat to olm populations. Despite the constant presence of microorganisms in their environment and the frequent occurrence of parasites in their tissues, the olm individuals in the natural environment tend to remain in good physical condition, which indicates the effectiveness of their defense mechanisms and their ability to defend themselves against naturally occurring parasites and pathogens. At the same time, the increased sensitivity of olms to pathogens and parasites under controlled conditions indicates a suboptimal response of their immune system, even under relatively moderate captive stress. In this respect, the increased susceptibility of olms to pathogens under the constant pressure of pollutants and other stressors in their natural environment (Bulog, 2007) represents a reasonable threat. In order to assess the severity of these indirect threats and the infestations rate of olm as an indicator of environmental condition, a survey on the occurrence of parasites in archived olm specimens was recently initiated. In addition to providing information on the occurrence of parasites in olms over the last five decades, the results of the survey may contribute to an objective assessment of the threat to natural populations of the olm and to the preparation of appropriate conservation measures.

Conservation The nominal species Proteus anguinus is protected in all range states including Montenegro, where its presence has only recently been indicated by eDNA. Internationally, P. anguinus is listed as vulnerable with a decreasing population trend on the IUCN Red List of Threatened Species (Arntzen et al., 2009), and it is protected as a priority species by the European Union Habitat Directive (Annex II, IV; Council of the European Communities, 1992). The Habitats Directive is a key instrument for conservation of biodiversity adopted in 1992 to protect habitats and species in freshwater, terrestrial and marine habitats in Europe. Although subterranean biodiversity is particularly diverse in Europe (Gibert and Culver 2009), only two more

IV. Principles of evolution in groundwater

Conservation

321

obligate subterranean species are included in the Habitats Directive: the terrestrial coleopteran Leptodirus hochenwartii and the bivalve Congeria kusceri. The cave bivalve is tiny and difficult to observe, so the olm’s role as a flagship species for the protection of groundwater ecosystems is underscored by its position in the EU legislation. The most important known olm sites within the EU member states Italy, Slovenia and Croatia are part of the Natura 2000 network of protected areas. However, the inclusion within Natura 2000 sites has contributed little to mitigate and eliminate threats and even to halt population decline. Examples of major threats include groundwater overpumping in Italy (Bressi, 2004), heavy organic pollution by farming and sewage in the subterranean Pivka river and the Kocevje area in Slovenia (Hudoklin, 2011), poisoning from heavy metals (Bulog et al., 2002) and illegally disposed polychlorinated biphenyl (PCB) waste at the Krupa karst spring in Slovenia (Pezdirc et al., 2011), habitat destruction through damming and artificial channeling of sinking rivers in the Trebisnjica and Neretva basin in Bosnia and Herzegovina (Aljancic et al., 2014). Most of these threats have severely affected olm populations causing local extinctions and drastic population decline. Besides these obvious major factors, many olm populations are facing a number of local threats with less clear effects. Examples are urbanization in catchment areas, poor wastewater treatment, landfills, small-scale farming with high usage of fertilizer and pesticides, altering of karst springs for various forms of human use, invasive changes to the landscape above karstic aquifers such as construction of roads and infrastructure or mining and limestone quarrying (Bressi, 2004; Hudoklin, 2016; Trontelj et al., 2017). Finally, direct pressure by collecting and disturbance has been known from the past and is emerging in new forms, e.g., as cave tourism and increased caving activity, but their impact has yet to be assessed. A common denominator of all but the most obvious and direct threats is that their impacts are difficult to assess and impossible to predict. There are three main reasons: (1) The actual position and extent of the olm’s subterranean habitat are unknown; what is mapped and formally protected are merely cave entrances or springs that might be kilometers away from the true habitat. (2) The hydrological connectivity between potential sources of pollution from the surface and the subterranean habitat are not well known, as are connections among habitat patches itself. (3) Because of the long lifecycles, low metabolism and relative robustness of adults, population size is believed to respond to worsened conditions with a delay of several years or decades. Early developmental stages that are most sensitive to pollution are usually hidden and cannot be monitored. One last point that importantly affects conservation strategies and priorities is the taxonomic subdivision of the genus Proteus For example, a small marginal population attracts little conservation attention as long as it is part of a species that has several strong and healthy populations. But if it turns out that this marginal population is the last survivor of a relict lineage or represents a distinct species, it may become top priority. Therefore, formalization of the taxonomic status of the nine known lineages of Proteus is under way. Already it is clear that these lineages differ substantially with respect to range size, population size and trends as well as exposure to threats (Table 13.1). It can be concluded that the lack of vision of how the species can be helped in places where it is believed to be declining and safeguard where it is still stable represents a major obstacle to effective conservation. In this sense, too, the olm is representative of groundwater biodiversity in general.

IV. Principles of evolution in groundwater

322

13. The olm (Proteus anguinus), a flagship groundwater species

Proteus lineages and/or evolutionarily significant units (ESU) as inferred from analyses of mtDNA sequences and nuclear DNA markers, along with estimated gross area, trend and threats.

TABLE 13.1

Lineage/ ESUa Kras/ Carso

Area Cumulative long-term (km2)b trendc 200

Ljubljanica 1100

Main conservation issues

Unknown; local decline Groundwater overpumping in the most western part of range; likely pollution from sinking Reka river; urbanization pressure, intensive agriculture Moderate decline

Sinking river pollution by agriculture and sewage; pollution from industry; cave tourism in the Postojna-Planina Cave System; excessive collecting in the past

Strong decline

Urbanization of the entire catchment area; destruction of habitat by construction and filling; groundwater pollution by diffuse infiltration of sewage and fertilizer; overcollecting in the past; inappropriate use of single remaining site by landowners

Dolenjska 1300

Moderate decline with local extinctions

Sinking river pollution by agriculture, sewage and industrial waste; illegal landfills and toxic waste dumps; groundwater pollution by diffuse infiltration of sewage and fertilizer

P. a. parkelj

Moderate to strong decline

Groundwater pollution by diffuse infiltration of sewage and fertilizer from local biogas plant, intensive agriculture and industrial waste dumps; urbanization and disturbance at karst springs

Sticna